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Glucosinolates pp 163-199 | Cite as

Regulation of Glucosinolate Metabolism: From Model Plant Arabidopsis thaliana to Brassica Crops

  • Rehna Augustine
  • Naveen C. BishtEmail author
Reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)

Abstract

Brassicaceae are blessed with secondary metabolites called glucosinolates which form the defense arsenal of these plants. Glucosinolates and its degradation products are also proved to be beneficial in agriculture and human health even though some are known to be detrimental. The type of glucosinolates and its content displays huge diversity across different species. The glucosinolate diversity is primarily genetically controlled. The profile of glucosinolates also varies depending on the growth stages and external environment of the plant. The environmental factors include type of pest/pathogen attack, nutrient status of the plant, and other abiotic stress factors. The glucosinolate pathway is also linked to other major metabolic and signaling pathways resulting in a complex mechanism of regulation. Even though the regulatory mechanism is not completely understood, the current chapter integrates the knowledge available from the model plant Arabidopsis and related Brassica crops.

Keywords

Brassica Glucosinolates Regulation Variability Differential accumulation Plant defense Sulfur deficiency Metabolic cross talk 

Abbreviations

ABA

Abscisic acid

BCAT

Branched-chain aminotransferases

CYP

Cytochrome P450

ET

Ethylene

FMO

Flavin monooxygenase

Glc

Glucose

GSL

Glucosinolate

GUS

β-Glucuronidase

HPLC

High-performance liquid chromatography

IPM

Isopropylmalate

JA

Jasmonic acid

MAM

Methylthioalkyl malate synthase

MeJA

Methyl jasmonic acid

Met

Methionine

QTL

Quantitative trait loci

Trp

Tryptophan

References

  1. 1.
    Beilstein MA, Al-Shehbaz IA, Kellogg EA (2006) Brassicaceae phylogeny and trichome evolution. Am J Bot 93:607–619CrossRefGoogle Scholar
  2. 2.
    Johnston JS, Pepper AE, Hall AE, Hodnett ZJCG, Drabek J, Lopez R, Price HJ (2005) Evolution of genome size in Brassicaceae. Ann Bot 95:229–235CrossRefGoogle Scholar
  3. 3.
    Augustine R, Arya GC, Nambiar DM, Kumar R, Bisht NC (2014) Translational genomics in Brassica crops: challenges, progress, and future prospects. Plant Biotechnol Rep 8:65–81CrossRefGoogle Scholar
  4. 4.
    Thangstad OP, Gilde B, Chadchawan S, Seem M, Husebye H, Bradley D, Bones AM (2004) Cell specific, cross-species expression of myrosinases in Brassica napus, Arabidopsis thaliana and Nicotiana tabacum. Plant Mol Biol 54:597–611CrossRefGoogle Scholar
  5. 5.
    Luthy B, Matile P (1984) The mustard oil bomb – rectified analysis of the subcellular organization of the myrosinase system. Boichem Physiol Pfl 179:5–12Google Scholar
  6. 6.
    Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333CrossRefGoogle Scholar
  7. 7.
    Clay NK, Adio AM, Carine C, Jander G, Ausubel FM (2009) GSL metabolites required for an Arabidopsis innate immune response. Science 323:95–101CrossRefGoogle Scholar
  8. 8.
    Hopkins RJ, Van Dam NM, Van Loon JJA (2009) Role of glucosinolates in insect plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83CrossRefGoogle Scholar
  9. 9.
    Cartea ME, Velasco P (2008) Glucosinolates in Brassica foods: bioavailability in food and significance for human health. Phytochem Rev 7:213–229CrossRefGoogle Scholar
  10. 10.
    Augustine R, Mukhopadhyay A, Bisht NC (2013) Targeted silencing of BjMYB28 transcription factor gene directs development of low glucosinolate lines in oilseed Brassica juncea. Plant Biotechnol J 11:855–886CrossRefGoogle Scholar
  11. 11.
    Yanaka FJW, Fukumoto A, Nakayama M, Inoue S, Zhang S, Tauchi M, Suzuki H, Hyodo I, Yamamoto M (2009) Dietary sulforaphane-rich broccoli sprouts reduce colonization and attenuate gastritis in Helicobacter pylori infected mice and humans. Cancer Prev Res 2:353–360CrossRefGoogle Scholar
  12. 12.
    Fahey JW, Wehage SL, Holtzclaw WD, Kensler TW, Egner PA, Shapiro TA, Talalay P (2012) Protection of humans by plant glucosinolates: efficiency of conversion of glucosinolates to isothiocyanates by the gastrointestinal microflora. Cancer Prev Res 5:603–611CrossRefGoogle Scholar
  13. 13.
    Sonderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates-gene discovery and beyond. Trends Plant Sci 15:283–290CrossRefGoogle Scholar
  14. 14.
    Agerbirk N, Olsen CE (2012) Glucosinolate structures in evolution. Phytochemistry 77:16–45CrossRefGoogle Scholar
  15. 15.
    Jensen LM, Kliebenstein DJ, Burow M (2015) Investigation of the multifunctional gene AOP3 expands the regulatory network fine-tuning glucosinolate production in Arabidopsis. Front Plant Sci 6:762Google Scholar
  16. 16.
    Diebold R, Schuster J, Daschner K, Binder S (2002) The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol 129:540–550CrossRefGoogle Scholar
  17. 17.
    Schuster J, Knill T, Reichelt M, Gershenzon J, Binder S (2006) Branched-chain aminotransferase 4 is part of the chain elongation pathway in the biosynthesis of methionine-derived glucosinolates in Arabidopsis. Plant Cell 18:2664–2679CrossRefGoogle Scholar
  18. 18.
    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 127:1077–1088CrossRefGoogle Scholar
  19. 19.
    Benderoth M, Textor S, Windsor AJ, Mitchell-Olds T, Gershenzon J, Kroymann J (2006) Positive selection driving diversification in plant secondary metabolism. Proc Natl Acad Sci U S A 103:9118–9123CrossRefGoogle Scholar
  20. 20.
    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 144:60–71CrossRefGoogle Scholar
  21. 21.
    He Y, Mawhinney TP, Preuss ML, Schroeder AC, Chen B, Abraham L, Jez JM, Chen S (2009) A redox-active isopropylmalate dehydrogenase functions in the biosynthesis of glucosinolates and leucine in Arabidopsis. Plant J 60:679–690CrossRefGoogle Scholar
  22. 22.
    Sawada Y, Kuwahara A, Nagano M, Narisawa T, Sakata A, Saito K, Hirai MY (2009) Omics-based approaches to methionine side chain elongation in Arabidopsis: characterization of gene encoding methylthioalkylmalate isomerase and methylthioalkylmalate dehydrogenase. Plant Cell Physiol 50:1180–1190Google Scholar
  23. 23.
    Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100CrossRefGoogle Scholar
  24. 24.
    Knill T, Schuster J, Reichelt M, Gershenzon J, Binder S (2008) Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol 146:1028–1039CrossRefGoogle Scholar
  25. 25.
    Gigolashvili T, Yatusevich R, Rollwitz I, Humphry M, Gershenzon J, Flugge UI (2009) The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21:1813–1829CrossRefGoogle Scholar
  26. 26.
    Hull AK, Vij R, Celenza JL (2000) Arabidopsis cytochrome P450s that catalyze the first step of tryptophan-dependent indole-3-acetic acid biosynthesis. Proc Natl Acad Sci U S A 97:2379–2384CrossRefGoogle Scholar
  27. 27.
    Chen S, Glawischning E, Jorgensen K, Naur P, Jorgensen B, Olsen CE, Hansen CH, Rasmussen H, Pickett JA, Halkier BA (2003) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J 33:923–937CrossRefGoogle Scholar
  28. 28.
    Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. catalyzes the conversion of Lphenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J Biol Chem 275:14659–14666CrossRefGoogle Scholar
  29. 29.
    Naur P, Petersen BL, Mikkelsen MD, Bak S, Rasmussen H, Olsen CE, Halkier BA (2003) CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133:63–72CrossRefGoogle Scholar
  30. 30.
    Wittstock U, Halkier BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 6:263–270CrossRefGoogle Scholar
  31. 31.
    Schlaeppi K, Bodenhausen N, Buchala A, Mauch F, Reymond P (2008) The glutathione-deficient mutant pad2-1 accumulates lower amounts of glucosinolates and is more susceptible to the insect herbivore Spodoptera littoralis. Plant J 55:774–786CrossRefGoogle Scholar
  32. 32.
    Mikkelsen MD, Naur P, Halkier BA (2004) Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. Plant J 37:770–777CrossRefGoogle Scholar
  33. 33.
    Grubb CD, Zipp BJ, Ludwig-Muller J, Masuno MN, Molinski TF, Abel S (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893–908CrossRefGoogle Scholar
  34. 34.
    Klein M, Reichelt M, Gershenzon J, Papenbrock J (2006) The three desulfoglucosinolate sulfotransferase proteins in Arabidopsis have different substrate specificities and are differentially expressed. FEBS J 273:122–136CrossRefGoogle Scholar
  35. 35.
    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 50:902–910CrossRefGoogle Scholar
  36. 36.
    Li J, Hansen BG, Ober JA, Kliebenstein DJ, Halkier BA (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol 148:1721–1733CrossRefGoogle Scholar
  37. 37.
    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 13:681–693CrossRefGoogle Scholar
  38. 38.
    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 126:811–825CrossRefGoogle Scholar
  39. 39.
    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 148:2096–2108CrossRefGoogle Scholar
  40. 40.
    Reichelt M, Brown PD, Schneider B, Oldham NJ, Stauber E, Tokuhisa J, Kliebenstein DJ, Mitchell-Olds T, Gershenzon J (2002) Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana. Phytochemistry 9(6):663–671CrossRefGoogle Scholar
  41. 41.
    Kliebenstein DJ, D’Auria J, Behere A, Kim J, Gunderson K, Breen J, Lee G, Gershenzon J, Last R, Jander G (2007) Characterization of seed-specific benzoyloxyglucosinolate mutations in Arabidopsis thaliana. Plant J 51:1062–1076CrossRefGoogle Scholar
  42. 42.
    Lee S, Kaminaga Y, Cooper B, Pichersky E, Dudareva N, Chapple C (2012) Benzoylation and sinapoylation of glucosinolate R-groups in Arabidopsis. Plant J 72:411–422CrossRefGoogle Scholar
  43. 43.
    Zang YX, Kim HU, Kim JA, Lim MH, Jin M, Lee SC, Kwon SJ, Lee SI, Hong JK, Park TH, Mun JH, Seol YJ, Hong SB, Park BS (2009) Genome-wide identification of glucosinolate synthesis genes in Brassica rapa. FEBS J 276:3559–3574CrossRefGoogle Scholar
  44. 44.
    Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin I, Zhao M, Yu J, Huang S, Wang X, Yue Z et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930Google Scholar
  45. 45.
    Yan X, Chen S (2007) Regulation of plant glucosinolate metabolism. Planta 226:1343–1352CrossRefGoogle Scholar
  46. 46.
    Bisht NC, Gupta V, Ramchiary N, Sodhi YS, Mukhopadhyay A, Arumugam N, Pental D, Pradhan AK (2009) Fine mapping of loci involved with glucosinolate biosynthesis in oilseed mustard (Brassica juncea) using genomic information from allied species. Theor Appl Genet 118:413–421CrossRefGoogle Scholar
  47. 47.
    Wang H, Wu J, Sun S, Liu B, Cheng F, Sun R, Wang X (2011) Glucosinolate biosynthetic genes in Brassica rapa. Gene 487:135–142CrossRefGoogle Scholar
  48. 48.
    Li G, Quiros CF (2003) In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSLALK. Theor Appl Genet 106:1116–1121CrossRefGoogle Scholar
  49. 49.
    Liu Z, Hammerlindl J, Keller W, McVetty PBE, Daayf F, Quiros CF, Li G (2011) MAM gene silencing leads to the induction of C3 and reduction of C4 and C5 side-chain aliphatic glucosinolates in Brassica napus. Mol Breed 27:467–478CrossRefGoogle Scholar
  50. 50.
    Liu Z, Hirani AH, McVetty PBE, Daayf F, Quiros CF, Li G (2012) Reducing progoitrin and enriching glucoraphanin in Brassica napus seeds through silencing of the GSL-ALK gene family. Plant Mol Biol 79:179–189CrossRefGoogle Scholar
  51. 51.
    Zhu B, Wang Z, Yang J, Zhu Z, Wang H (2012) Isolation and expression of glucosinolate synthesis genes CYP83A1 and CYP83B1 in Pak Choi (Brassica rapa L. ssp. chinensis var. communis (N. Tsen & S.H. Lee) Hanelt). Int J Mol Sci 13(5):5832–5843CrossRefGoogle Scholar
  52. 52.
    Meenu AR, Majee M, Pradhan AK, Bisht NC (2015) Genomic origin, expression differentiation and regulation of multiple genes encoding CYP83A1, a key enzyme for core glucosinolate biosynthesis, from the allotetraploid Brassica juncea. Planta 241:651–665CrossRefGoogle Scholar
  53. 53.
    Wiesner M, Schreiner M, Zrenner R (2014) Functional identification of genes responsible for the biosynthesis of 1-methoxy-indol-3-ylmethyl-glucosinolate in Brassica rapa ssp. chinensis. BMC Plant Biol 8:114–124Google Scholar
  54. 54.
    Qu CM, Li SM, Duan XJ, Fan JH, Jia LD, Zhao HY, Lu K, Li JN, Xu XF, Wang R (2015) Identification of candidate genes for seed glucosinolate content using association mapping in Brassica napus L. Genes (Basel) 6(4):1215–1229Google Scholar
  55. 55.
    Augustine R, Bisht NC (2015) Biofortification of oilseed Brassica juncea with the anti-cancer compound glucoraphanin by suppressing the GSL-ALK gene family. Sci Rep 5:18005CrossRefGoogle Scholar
  56. 56.
    Guo L, Yang R, Gu Z (2016) Cloning of genes related to aliphatic glucosinolate metabolism and the mechanism of sulforaphane accumulation in broccoli sprouts under jasmonic acid treatment. J Sci Food Agric. doi:10.1002/jsfa.7629Google Scholar
  57. 57.
    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 43:79–96CrossRefGoogle Scholar
  58. 58.
    Blume B, Nurnberger T, Nass N, Scheel D (2000) Receptor mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425–1440CrossRefGoogle Scholar
  59. 59.
    Maruyama-Nakashita A, Nakamura Y, Tohge T, Saito K, Takahashi H (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251CrossRefGoogle Scholar
  60. 60.
    Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184CrossRefGoogle Scholar
  61. 61.
    Frerigmann H, Gigolashvili T (2014) Update on the role of R2R3-MYBs in the regulation of glucosinolates upon sulfur deficiency. Front Plant Sci 5:626Google Scholar
  62. 62.
    Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, Zanor MI, Gershenzon J, Strnad M, Szopa J, Mueller-Roeber B, Witt I (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47:10–24CrossRefGoogle Scholar
  63. 63.
    Kang HG, Singh KB (2000) Characterization of salicylic acid-responsive, Arabidopsis DOF domain proteins: over-expression of OBP3 leads to growth defects. Plant J 21:329–339CrossRefGoogle Scholar
  64. 64.
    Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 10:573–581CrossRefGoogle Scholar
  65. 65.
    Gigolashvili T, Berger B, Flugge UI (2009) Specific and coordinated control of indole and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana. Phytochem Rev 8:3–13CrossRefGoogle Scholar
  66. 66.
    Zhang Y, Li B, Huai D, Zhou Y, Kliebenstein DJ (2015) The conserved transcription factors, MYB115 and MYB118, control expression of the newly evolved benzoyloxy glucosinolate pathway in Arabidopsis thaliana. Front Plant Sci 6:343Google Scholar
  67. 67.
    Bender J, Fink GR (1998) A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc Natl Acad Sci U S A 95:5655–5660CrossRefGoogle Scholar
  68. 68.
    Celenza JL, Quiel JA, Smolen GA, Merrikh H, Silvestro AR, Normanly J, Bender J (2005) The Arabidopsis ATR1Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 137:253–262CrossRefGoogle Scholar
  69. 69.
    Gigolashvili T, Berger B, Mock HP, Muller C, Weisshaar B, Flugge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901CrossRefGoogle Scholar
  70. 70.
    Frerigmann H, Gigolashvili T (2014) MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol Plant 7:814–828CrossRefGoogle Scholar
  71. 71.
    Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuk A, Araki R, Sakurai N, Suzuki H, Aoki K, Goda H, Nishizawa OI, Shibata D, Saito K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic GSL biosynthesis. Proc Natl Acad Sci U S A 104:6478–6483CrossRefGoogle Scholar
  72. 72.
    Gigolashvili T, Yatusevich R, Berger B, Muller C, Flugge UI (2007) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51:247–261CrossRefGoogle Scholar
  73. 73.
    Gigolashvili T, Engqvist M, Yatusevich R, Muller C, Flugge 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 177:627–642CrossRefGoogle Scholar
  74. 74.
    Sønderby IE, Hansen BG, Bjarnholt N, Ticconi C, Halkier BA, Kliebenstein DJ (2007) A systems biology approach identifies a R2R3MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolate. PLoS One 2, e1322CrossRefGoogle Scholar
  75. 75.
    Augustine R, Bisht NC (2015) Biotic elicitors and mechanical damage modulate glucosinolate accumulation by co-ordinated interplay of glucosinolate biosynthesis regulators in polyploid Brassica juncea. Phytochemistry 117:43–50CrossRefGoogle Scholar
  76. 76.
    Li Y, Sawada Y, Hirai A, Sato M, Kuwahara A, Yan X, Hirai MY (2013) Novel insights into the function of Arabidopsis R2R3-Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Plant Cell Physiol 54(8):1335–1344CrossRefGoogle Scholar
  77. 77.
    Kim B, Li X, Kim SJ, Kim HH, Lee J, Kim HR, Park SU (2013) MYB Transcription factors regulate glucosinolate biosynthesis in different organs of Chinese Cabbage (Brassica rapa ssp. pekinensis). Molecules 18:8682–8695CrossRefGoogle Scholar
  78. 78.
    Araki R, Hasumi A, Nishizawa OI, Sasaki K, Kuwahara A, Sawada Y, Totoki Y, Toyoda A, Sakaki Y, Li Y, Saito K, Ogawa T, Hirai MY (2013) Novel bioresources for studies of Brassica oleracea: identification of a kale MYB transcription factor responsible for glucosinolate production. Plant Biotechnol J 11:1017–1027CrossRefGoogle Scholar
  79. 79.
    Hsu FC, Wirtz M, Heppel SC, Bogs J, Krämer U, Khan MS, Bub A, Hell R, Rausch T (2011) Generation of Se-fortified broccoli as functional food: impact of Se fertilization on S metabolism. Plant Cell Environ 34:192–207CrossRefGoogle Scholar
  80. 80.
    Yi GE, Robin AHK, Yang K, Park JI, Kang JG, Yang TJ, Nou IS (2015) Identification and Expression analysis of glucosinolate biosynthetic genes and estimation of glucosinolate contents in edible organs of Brassica oleracea subspecies. Molecules 20:13089–13111CrossRefGoogle Scholar
  81. 81.
    Augustine R, Majee M, Gershenzon J, Bisht NC (2013) Four genes encoding MYB28, a major transcriptional regulator of aliphatic glucosinolate pathway, are differentially expressed in the allopolyploid Brassica juncea. J Exp Bot 64:4907–4921CrossRefGoogle Scholar
  82. 82.
    Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymonda P (2013) Arabidopsis basic Helix-Loop-Helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis insect performance, and feeding behavior. Plant Cell 25:3117–3132CrossRefGoogle Scholar
  83. 83.
    Fernández-Calvo P, Chini A, Fernández-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM, Pauwels L, Witters E, Puga MI, Paz-Ares J, Goossens A, Reymond P, De Jaeger G, Solano R (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715CrossRefGoogle Scholar
  84. 84.
    Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse jasmonate dependent functions in Arabidopsis. Plant Cell 19:2225–2245CrossRefGoogle Scholar
  85. 85.
    Parkin I, Magrath R, Keith D, Sharpe A, Mithen R, Lydiate D (1994) Genetics of aliphatic glucosinolates. II. Hydroxylation of alkenyl glucosinolates in Brassica napus. Heredity 72:594–598CrossRefGoogle Scholar
  86. 86.
    Mithen RF, Clarke J, Lister C, Dean C (1995) Genetics of aliphatic glucosinolates. III. Side chain structure of aliphatic glucosinolates in Arabidopsis thaliana. Heredity 74:210–215CrossRefGoogle Scholar
  87. 87.
    Giamoustaris A, Mithen R (1996) Genetics of aliphatic glucosinolates IV Side-chain modification in Brassica oleracea. Theor Appl Genet 93:1006–1010CrossRefGoogle Scholar
  88. 88.
    Zhang J, Wang X, Cheng F, Wu J, Liang J, Yang W, Wang X (2015) Lineage-specific evolution of Methylthioalkylmalate synthases (MAMs) involved in glucosinolates biosynthesis. Front Plant Sci 6:18Google Scholar
  89. 89.
    Neal CS, Fredericks DP, Griffiths CA, Neale AD (2010) The characterization of AOP2: a gene associated with biosynthesis of aliphatic alkenyl glucosinolates in Arabidopsis thaliana. BMC Plant Biol 10:170–186CrossRefGoogle Scholar
  90. 90.
    Rohr F, Ulrichs C, Schreiner M, Zrenner R, Mewis I (2012) Responses of Arabidopsis thaliana plant lines differing in hydroxylation of aliphatic glucosinolate side chains to feeding of a generalist and specialist caterpillar. Plant Physiol Biochem 55:52–59CrossRefGoogle Scholar
  91. 91.
    Burow M, Atwell S, Francisco M, Kerwin RE, Halkier BA, Kliebenstein DJ (2015) The Glucosinolate biosynthetic gene AOP2 mediates feed-back regulation of jasmonic acid signaling in Arabidopsis. Mol Plant 8:1201–1212CrossRefGoogle Scholar
  92. 92.
    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, e162CrossRefGoogle Scholar
  93. 93.
    Kliebenstein DJ, Gershenzon J, Mitchell-Olds T (2001) Comparative quantitative trait loci mapping of aliphatic, indole and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159:359–370Google Scholar
  94. 94.
    van Doorn HE, van der Kruk GC, van Holst GJ, Raaijmakers-Ruijs NCME, Postma E, Groeneweg B, Jongen WHF (1998) The glucosinolates sinigrin and progoitrin are important determinants for taste preference and bitterness of Brussels sprouts. J Sci Food Agric 78:30–38CrossRefGoogle Scholar
  95. 95.
    Wentzell AM, Kliebenstein DJ (2008) Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiol 147:415–428CrossRefGoogle Scholar
  96. 96.
    van Dam NM, Tytgat TOG, Kirkegaard JA (2009) Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochem Rev 8:171–186CrossRefGoogle Scholar
  97. 97.
    Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481CrossRefGoogle Scholar
  98. 98.
    Baskar V, Park SW (2015) Molecular characterization of BrMYB28 and BrMYB29 paralogous transcription factors involved in the regulation of aliphatic glucosinolate profiles in Brassica rapa ssp. pekinensis. C R Bio 338(7):434–442CrossRefGoogle Scholar
  99. 99.
    Tierens KF, Thomma BP, Brouwer M, Schmidt J, Kistner K, Porzel A, Mauch-Mani B, Cammue BP, Broekaert WF (2001) Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol 125:1688–1699CrossRefGoogle Scholar
  100. 100.
    Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019CrossRefGoogle Scholar
  101. 101.
    Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106CrossRefGoogle Scholar
  102. 102.
    Sotelo T, Lema M, Soengas P, Cartea ME, Velasco P (2015) In vitro activity of glucosinolates and their degradation products against Brassica-pathogenic bacteria and fungi. Appl Environ Microbiol 81:432–440CrossRefGoogle Scholar
  103. 103.
    Lankau RA, Kliebenstein DJ (2009) Competition, herbivory and genetics interact to determine the accumulation and fitness consequences of a defense metabolite. J Ecol 97:78–88CrossRefGoogle Scholar
  104. 104.
    Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signalling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects. Plant Physiol 138:1149–1162CrossRefGoogle Scholar
  105. 105.
    Mewis I, Tokuhisa JG, Schultz JC, Appel HM, Ulrichs C, Gershenzon J (2006) Gene expression and glucosinolate accumulation in Arabidopsis thaliana in response to generalist and specialist herbivores of different feeding guilds and the role of defense signaling pathways. Phytochemistry 67(22):2450–2462CrossRefGoogle Scholar
  106. 106.
    Kusnierczyk A, Winge P, Midelfart H, Armbruster WS, Rossiter JT, Bones AM (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J Exp Bot 58(10):2537–2552CrossRefGoogle Scholar
  107. 107.
    Badenes-Perez FR, Reichelt M, Gershenzon J, Heckel DG (2013) Interaction of glucosinolate content of Arabidopsis thaliana mutant lines and feeding and oviposition by generalist and specialist lepidopterans. Phytochemistry 86:36–43CrossRefGoogle Scholar
  108. 108.
    Appel HM, Maqbool SB, Raina S, Jagadeeswaran G, Acharya BR, Hanley JC Jr, Miller KP, Hearnes L, Jones AD, Raina R, Schultz JC (2014) Transcriptional and metabolic signatures of Arabidopsis responses to chewing damage by an insect herbivore and bacterial infection and the consequences of their interaction. Front Plant Sci 5:441Google Scholar
  109. 109.
    Ahuja I, van Dam NM, Winge P, Traelnes M, Heydarova A, Rohloff J, Langaas M, Bones AM (2015) Plant defence responses in oilseed rape MINELESS plants after attack by the cabbage moth Mamestra brassicae. J Exp Bot 66:579–592CrossRefGoogle Scholar
  110. 110.
    Schlaeppi K, Abou-Mansour E, Buchala A, Mauch F (2010) Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J 62(5):840–851CrossRefGoogle Scholar
  111. 111.
    Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5(6):1389–1402CrossRefGoogle Scholar
  112. 112.
    van de Mortel JE, de Vos RC, Dekkers E, Pineda A, Guillod L, Bouwmeester K, van Loon JJ, Dicke M, Raaijmakers JM (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160(4):2173–2188CrossRefGoogle Scholar
  113. 113.
    Wei L, Jian H, Lu K, Filardo F, Yin N, Liu L, Qu C, Li W, Du H, Li J (2015) Genome-wide association analysis and differential expression analysis of resistance to Sclerotinia stem rot in Brassica napus. Plant Biotechnol J. doi:10.1111/pbi.12501Google Scholar
  114. 114.
    Velasco P, Lema M, Francisco M, Soengas P, Cartea ME (2013) In vivo and in vitro effects of secondary metabolites against Xanthomonas campestris pv. campestris. Molecules 18(9):11131–11143CrossRefGoogle Scholar
  115. 115.
    Zhang Y, Huai D, Yang Q, Cheng Y, Ma M, Kliebenstein DJ, Zhou Y (2015) Overexpression of three glucosinolate biosynthesis genes in Brassica napus identifies enhanced resistance to Sclerotinia sclerotiorum and Botrytis cinerea. PLoS One 10(10), e0140491CrossRefGoogle Scholar
  116. 116.
    Kiddle GA, Doughty KJ, Wallsgrove RM (1994) Salicylic acid induced accumulation of glucosinolates in oilseed rape (Brassica napus L.) leaves. J Exp Bot 45:1343–1346CrossRefGoogle Scholar
  117. 117.
    Doughty KJ, Porter AJR, Morton AM, Kiddle G, Bock CH, Wallsgrove R (1991) Variation in the glucosinolate content of oilseed rape (Brassica napus L). Ann Appl Biol 118:469–477CrossRefGoogle Scholar
  118. 118.
    Brader G, Tas E, Palva ET (2001) Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the non specific pathogen Erwinia carotovora. Plant Physiol 126:849–860CrossRefGoogle Scholar
  119. 119.
    Mikkelsen MD, Petersen BL, Glawischnig E, Jensen AB, Andreasson E, Halkier BA (2003) Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol 131:298–308CrossRefGoogle Scholar
  120. 120.
    Glazebrook J, Chen W, Esters B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228CrossRefGoogle Scholar
  121. 121.
    Tauzin AS, Giardina T (2014) Sucrose and invertases, a part of the plant defense response to the biotic stresses. Front Plant Sci 5:293CrossRefGoogle Scholar
  122. 122.
    Li YH, Lee KK, Walsh S, Smith C, Hadingham S, Sorefan K, Cawley G, Bevan MW (2006) Establishing glucose- and ABA-regulated transcription networks in Arabidopsis by microarray analysis and promoter classification using a relevance vector machine. Genome Res 16:414–427CrossRefGoogle Scholar
  123. 123.
    Miao HY, Wei J, Zhao YT, Yan HZ, Sun B, Huang JR, Wang Q (2013) Glucose signalling positively regulates aliphatic glucosinolate biosynthesis. J Exp Bot 64:1097–1109CrossRefGoogle Scholar
  124. 124.
    Guo R, Shen W, Qian H, Zhang M, Liu L, Wang Q (2013) Jasmonic acid and glucose synergistically modulate the accumulation of glucosinolates in Arabidopsis thaliana. J Exp Bot 64:5707–5719CrossRefGoogle Scholar
  125. 125.
    Guo R, Qian H, Shen W, Liu L, Zhang M, Cai C, Zhao Y, Qiao J, Wang Q (2013) BZR1 and BES1 participate in regulation of glucosinolate biosynthesis by brassinosteroids in Arabidopsis. J Exp Bot 64(8):2401–2412CrossRefGoogle Scholar
  126. 126.
    Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719CrossRefGoogle Scholar
  127. 127.
    Bodnaryk RP (1992) Effects of wounding on glucosinolates in the cotyledons of oilseed rape and mustard. Phytochemistry 31:2671–2677CrossRefGoogle Scholar
  128. 128.
    Wiesner M, Hanschen FS, Schreiner M, Glatt H, Zrenner R (2013) Induced production of 1-methoxy-indol-3-ylmethyl glucosinolate by jasmonic acid and methyl jasmonate in sprouts and leaves of pak choi (Brassica rapa ssp. chinensis). Int J Mol Sci 14:14996–15016CrossRefGoogle Scholar
  129. 129.
    Baenas N, Garcia-Viguera C, Moreno DA (2014) Biotic elicitors effectively increase the glucosinolates content in Brassicaceae sprouts. J Agric Food Chem 62:1881–1889CrossRefGoogle Scholar
  130. 130.
    Fagard M, Launay A, Clément G, Courtial J, Dellagi A, Farjad M, Krapp A, Soulié M-C, Masclaux-Daubresse C (2014) Nitrogen metabolism meets phytopathology. J Exp Bot 65:5643–5656CrossRefGoogle Scholar
  131. 131.
    Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plantarum 133:682–691CrossRefGoogle Scholar
  132. 132.
    Liang G, He H, Yu D (2012) miR826, a newly identified N-starvation-induced miRNA, was found to target the AOP2 gene identification of nitrogen starvation-responsive MicroRNAs in Arabidopsis thaliana. PLoS One 7(11):e48951CrossRefGoogle Scholar
  133. 133.
    He H, Liang G, Li Y, Wang F, Yu D (2014) Two young MicroRNAs originating from target duplication mediate nitrogen starvation adaptation via regulation of glucosinolate synthesis in Arabidopsis thaliana. Plant Physiol 164(2):853–865CrossRefGoogle Scholar
  134. 134.
    Troufflard S, Mullen W, Larson TR, Graham IA, Crozier A, Amtmann A, Armengaud P (2010) Potassium deficiency induces the biosynthesis of oxylipins and glucosinolates in Arabidopsis thaliana. BMC Plant Biol 10:172CrossRefGoogle Scholar
  135. 135.
    Falk KL, Tokuhisa JG, Gershenzon J (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol 9(5):573–581CrossRefGoogle Scholar
  136. 136.
    Nikiforova V, Freitag J, Kempa S, Adamik M, Hesse H, Hoefgen R (2003) Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33:633–650CrossRefGoogle Scholar
  137. 137.
    Schonhof I, Blankenburg D, Muller S, Krumbein A (2007) Sulfur and nitrogen supply influence growth, product appearance, and glucosinolate concentration of broccoli. J Plant Nutr Soil Sci 170:65–72CrossRefGoogle Scholar
  138. 138.
    Zhao F, Evans EJ, Bilsborrow PE, Syers JK (1994) Influence of nitrogen and sulphur on the glucosinolate profile of rapeseed (Brassica napus L). J Sci Food Agri 64:295–304CrossRefGoogle Scholar
  139. 139.
    Kim SJ, Matsuo T, Watannabe M, Watannabe Y (2002) Effect of nitrogen and sulphur application on the glucosinolate concentration in vegetable turnip rape (Brassica rapa L). Soil Sci Plant Nutr 48:43–49CrossRefGoogle Scholar
  140. 140.
    Omirou MD, Papadopoulou KK, Papastylianou I, Constantinou M, Karpouzas DG, Asimakopoulos I, Ehaliotis C (2009) Impact of nitrogen and sulfur fertilization on the composition of glucosinolates in relation to sulfur assimilation in different plant organs of broccoli. J Agric Food Chem 57(20):9408–9417CrossRefGoogle Scholar
  141. 141.
    Maruyama-Nakashita A, Inoue E, Watanabe-Takahashi A, Yamaya T, Takahashi H (2003) Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132:597–605CrossRefGoogle Scholar
  142. 142.
    Hirai MY, Klein M, Fujikawa Y, Yano M, Goodenowe DB, Yamazaki Y, Kanaya S, Nakamura Y, Kitayama M, Suzuki H, Sakurai N, Shibata D, Tokuhisa J, Reichelt M, Gershenzon J, Papenbrock J, Saito K (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in Arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595CrossRefGoogle Scholar
  143. 143.
    Yatusevich R, Mugford SG, Matthewman C, Gigolashvili T, Frerigmann H, Delaney S et al (2009) Genes of primary sulfate assimilation are part of the glucosinolate biosynthetic network in Arabidopsis thaliana. Plant J 62:1–11CrossRefGoogle Scholar
  144. 144.
    Vadassery J, Reichelt M, Hause B, Gershenzon J, Boland W, Mithöfer A (2012) CML42-mediated calcium signaling coordinates responses to Spodoptera herbivory and abiotic stresses in Arabidopsis. Plant Physiol 159:1159–1175CrossRefGoogle Scholar
  145. 145.
    Ide Y, Kusano M, Oikawa A, Fukushima A, Tomatsu H, Saito K, Hirai MY, Fujiwara T (2011) Effects of molybdenum deficiency and defects in molybdate transporter MOT1 on transcript accumulation andnitrogen/sulphur metabolism in Arabidopsis thaliana. J Exp Bot 62(4):1483–1497CrossRefGoogle Scholar
  146. 146.
    Kim HS, Juvik JA (2011) Effect of selenium fertilization and methyl jasmonate treatment on glucosinolate accumulation in broccoli florets. J Am Soc Hort Sci 136:239–246Google Scholar
  147. 147.
    Avila FW, Yang Y, Faquin V, Ramos SJ, Guilherme LR, Thannhauser TW, Li L (2014) Impact of selenium supply on Se-methylselenocysteine and glucosinolate accumulation in selenium-biofortified Brassica sprouts. Food Chem 165:578–586CrossRefGoogle Scholar
  148. 148.
    Shelp BJ, Shattuck VI, McLellan D, Liu L (1992) Boron nutrition and the composition of glucosinolates and soluble nitrogen compounds in two broccoli (Brassica oleracea var. italica) cultivars. Can J Plant Sci 72:889–899CrossRefGoogle Scholar
  149. 149.
    Kusznierewicz B, Bączek-Kwinta R, Bartoszek A, Piekarska A, Huk A, Manikowska A, Antonkiewicz J, Namieśnik J, Konieczka P (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolatecontent in white cabbage (Brassica oleracea var. capitata f. alba). Environ Toxicol Chem 31(11):2482–2489CrossRefGoogle Scholar
  150. 150.
    Martínez-Ballesta MC, Moreno DA, Carvajal M (2013) The physiological importance of glucosinolates on plant response to abiotic stress in Brassica. Int J Mol Sci 14:11607–11625CrossRefGoogle Scholar
  151. 151.
    Justen VL, Fritz VA (2013) Temperature-induced glucosinolate accumulation is associated with expression of BrMYB transcription factors. Hortscience 48:47–52Google Scholar
  152. 152.
    Johansen TJ, Hagen SF, Bengtsson GB, Mølmann JA (2016) Growth temperature affects sensory quality and contents of glucosinolates, vitamin C and sugars in swede roots (Brassica napus L. ssp. rapifera Metzg.). Food Chem 1(196):228–235CrossRefGoogle Scholar
  153. 153.
    Huseby S, Koprivova A, Lee BR, Saha S, Mithen R, Wold AB, Bengtsson GB, Kopriva S (2013) Diurnal and light regulation of sulphur assimilation and glucosinolate biosynthesis in Arabidopsis. J Exp Bot 64(4):1039–1048CrossRefGoogle Scholar
  154. 154.
    Kim YB, Chun JH, Kim HR, Kim SJ, Lim YP, Park SU (2014) Variation of glucosinolate accumulation and gene expression of transcription factors at different stages of Chinese cabbage seedlings under light and dark conditions. Nat Prod Commun 9(4):533–537Google Scholar
  155. 155.
    Schonhof I, Klaring HP, Krumbein A, Schreiner M (2007) Interaction between atmospheric CO2 and glucosinolates in broccoli. J Chem Ecol 33:105–114CrossRefGoogle Scholar
  156. 156.
    La GX, Fang P, Teng YB, Li YJ, Lin XY (2009) Effect of CO2 enrichment on the glucosinolate contents under different nitrogen levels in bolting stem of Chinese kale (Brassica alboglabra L.). J Zhejiang Univ Sci B 10(6):454–464CrossRefGoogle Scholar
  157. 157.
    Radovich TJK, Kleinhenz MD, Streeter JG (2005) Irrigation timing relative to head development influences yield components, sugar levels, and glucosinolate concentrations in cabbage. J Am Soc Hortic Sci 130:943–949Google Scholar
  158. 158.
    Schreiner M, Beyene B, Krumbein A, Stutzel H (2009) Ontogenetic changes of 2-propenyl and 3-indolylmethyl glucosinolates in Brassica carinata leaves as affected by water supply. J Agric Food Chem 57:7259–7263CrossRefGoogle Scholar
  159. 159.
    Steinbrenner AD, Agerbirk N, Orians CM, Chew FS (2012) Transient abiotic stresses lead to latent defense and reproductive responses over the Brassica rapa life cycle. Chemoecology 22:239–250CrossRefGoogle Scholar
  160. 160.
    Guo RF, Yuan GF, Wang QM (2013) Effect of NaCl treatments on glucosinolate metabolism in broccoli sprouts. J Zhejiang Univ Sci B 14(2):124–131CrossRefGoogle Scholar
  161. 161.
    Velasco P, Cartea ME, Gonzalez C, Vilar M, Ordas A (2007) Factors affecting the glucosinolate content of kale (Brassica oleracea acephala group). J Agric Food Chem 55:955–962CrossRefGoogle Scholar
  162. 162.
    Reintanz B, Lehnen M, Reichelt M, Gershenzon J, Kowalczyk M, Sandberg G, Godde M, Uhl R, Pame K (2001) bus, a bushy Arabidopsis CYP79F1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13:351–367CrossRefGoogle Scholar
  163. 163.
    Bak S, Tax FE, Feldmann KA, Galbraith DW, Feyereisen R (2001) CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:101–111CrossRefGoogle Scholar
  164. 164.
    Sugawara S, Hishiyama S, Jikumaru Y, Hanada A, Nishimura T, Koshiba T, Kamiya Y, Kasahara H (2009) Biochemical analyses of indole-3-acetaldoxime-dependent auxin biosynthesis in Arabidopsis. Proc Natl Acad Sci U S A 106(13):5430–5435CrossRefGoogle Scholar
  165. 165.
    Glawischnig E, Hansen BG, Olsen CE, Halkier BA (2004) Camalexin is synthesized from indole-3-acetaidoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc Natl Acad Sci U S A 101:8245–8250CrossRefGoogle Scholar
  166. 166.
    Hemm MR, Ruegger MO, Chapple C (2003) The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glucosinolate phenotypes. Plant Cell 15(1):179–194CrossRefGoogle Scholar
  167. 167.
    Kim JI, Dolan WL, Anderson NA, Chapple C (2015) Indole glucosinolate biosynthesis limits phenylpropanoid accumulation in Arabidopsis thaliana. Plant Cell 27(5):1529–1546CrossRefGoogle Scholar
  168. 168.
    Malitsky S, Blum E, Less H, Venger I, Elbaz M, Morin S, Eshed Y, Aharoni A (2008) The transcript and metabolite networks affected by the two clades of Arabidopsis glucosinolate biosynthesis regulators. Plant Physiol 148:2021–2049CrossRefGoogle Scholar
  169. 169.
    Kong W, Li Y, Zhang M, Jin F, Li J (2015) A novel Arabidopsis microRNA promotes IAA biosynthesis via the indole-3-acetaldoxime pathway by suppressing superroot1. Plant Cell Physiol 56(4):715–726CrossRefGoogle Scholar
  170. 170.
    Chen S, Petersen BL, Olsen CE, Schulz A, Halkier BA (2001) Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol 127:194–201CrossRefGoogle Scholar
  171. 171.
    Nour-Eldin HH, Andersen TG, Burow M, Madsen SR, Jørgensen ME, Olsen CE, Dreyer I, Hedrich R, Geiger D, Halkier BA (2012) NRT/PTR transporters are essential for translocation of glucosinolate defence compounds to seeds. Nature 488(7412):531–534CrossRefGoogle Scholar
  172. 172.
    Koroleva OA, Gibson TM, Cramer R, Stain C (2010) Glucosinolate-accumulating S-cells in Arabidopsis leaves and flower stalks undergo programmed cell death at early stages of differentiation. Plant J 64(3):456–469CrossRefGoogle Scholar
  173. 173.
    Wittstock U, Burow M (2010) Glucosinolate breakdown in Arabidopsis: mechanism, regulation and biological significance. Arabidopsis Book 8, e0134CrossRefGoogle Scholar
  174. 174.
    Xu Z, Escamilla-Trevino LL, Zeng L, Lalgondar M, Bevan DR, Winkel BSJ, Mohamed A, Cheng C-L, Shih M-C, Poulton JE, Esen A (2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol Biol 55:343–367CrossRefGoogle Scholar
  175. 175.
    Rask L, Andreasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J (2000) Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol 42:93–113CrossRefGoogle Scholar
  176. 176.
    Lenman M, Falk A, Roedin J, Hoeglund A-S, Ek B, Rask L (1993) Differential expression of myrosinase gene families. Plant Physiol 103:703–711CrossRefGoogle Scholar
  177. 177.
    Kissen R, Hyldbakk E, Wang CWV, Sormo CG, Rossiter JT, Bones AM (2012) Ecotype dependent expression and alternative splicing of epithiospecifier protein (ESP) in Arabidopsis thaliana. Plant Mol Biol 78:361–375CrossRefGoogle Scholar
  178. 178.
    Kissen R, Bones AM (2009) Nitrile-specifier proteins involved in glucosinolate hydrolysis in Arabidopsis thaliana. J Biol Chem 284:12057–12070CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.National Institute of Plant Genome Research (NIPGR)New DelhiIndia

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