Abstract
In plants the amino acid tryptophan (Trp) is used to synthesize proteins and a wide variety of compounds that control development and defense. Recent studies in the reference plant Arabidopsis thaliana have elucidated a number of tryptophan secondary metabolism pathways derived from the Trp metabolite, indole-3-acetaldoxime (IAOx), particularly the pathway for synthesis of indolic glucosinolate (IG) herbivory defense compounds. Analyses of mutants, natural variants, and transgenic strains with perturbations in the IG pathway have revealed that regulation of this pathway is networked at many levels, including interfaces with Trp synthesis, other Trp secondary metabolism pathways, other glucosinolate synthesis pathways, and sulfur metabolism. Transcriptional regulatory mechanisms have been particularly well characterized, but additional mechanisms such as metabolic channeling may also contribute to the homeostasis of Trp secondary metabolism. The IG pathway thus serves as a paradigm for regulatory cross-talk between primary and secondary metabolism and among inter-related secondary metabolic processes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AS:
-
Anthranilate synthase
- atr:
-
Altered Trp regulation
- bHLH:
-
Basic helix-loop-helix
- I3M:
-
Indol-3-ylmethyl glucosinolate
- IAA:
-
Indole-3-acetic acid
- IAN:
-
Indole-3-acetonitrile
- IAOx:
-
Indole-3-acetaldehyde
- IG:
-
Indolic glucosinolate
- 5MT:
-
5-Methyltryptophan
- Trp:
-
Tryptophan
References
Bak S, Feyereisen R (2001) The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiol 127:108–118. doi:10.1104/pp.127.1.108
Bak S, Tax FE, Feldmann KA et al (2001) CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:101–111
Bak S, Paquette S, Morant M et al (2006) Cyanogenic glycosides: a case study for evolution and application of cytochromes P450. Phytochem Rev 5:309–329. doi:10.1007/s11101-006-9033-1
Barlier I, Kowalczyk M, Marchant A et al (2000) The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. Proc Natl Acad Sci USA 97:14819–14824. doi:10.1073/pnas.260502697
Bartee L, Bender J (2001) Two Arabidopsis methylation-deficiency mutations confer only partial effects on a methylated endogenous gene family. Nucleic Acids Res 29:2127–2134. doi:10.1093/nar/29.10.2127
Bender J, Fink GR (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83:725–734. doi:10.1016/0092-8674(95)90185-X
Bender J, Fink GR (1998) A Myb homologue, ATR1, activates tryptophan gene expression in Arabidopsis. Proc Natl Acad Sci USA 95:5655–5660. doi:10.1073/pnas.95.10.5655
Boerjan W, Cervera MT, Delarue M et al (1995) Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. Plant Cell 7:1405–1419
Bones AM, Rossiter JT (2006) The enzymic and chemically induced decomposition of glucosinolates. Phytochemistry 67:1053–1067. doi:10.1016/j.phytochem.2006.02.024
Brown PD, Tokuhisa JG, Reichelt M et al (2003) Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62:471–481. doi:10.1016/S0031-9422(02)00549-6
Celenza JL Jr, Grisafi PL, Fink GR (1995) A pathway for lateral root formation in Arabidopsis thaliana. Genes Dev 9:2131–2142. doi:10.1101/gad.9.17.2131
Celenza JL, Quiel JA, Smolen GA et al (2005) The Arabidopsis ATR1 Myb transcription factor controls indolic glucosinolate homeostasis. Plant Physiol 137:253–262. doi:10.1104/pp.104.054395
Chen S, Glawischnig E, Jorgensen K et al (2003) CYP79F1 and CYP79F2 have distinct functions in the biosynthesis of aliphatic glucosinolates in Arabidopsis. Plant J 33:923–937. doi:10.1046/j.1365-313X.2003.01679.x
Delarue M, Prinsen E, Van Onckelen H et al (1998) sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J 14:603–611. doi:10.1046/j.1365-313X.1998.00163.x
de Vos M, Kriksunov KL, Jander G (2008) Indole-3-Acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae. Plant Physiol 146:916–926. doi:10.1104/pp.107.112185
Dombrecht B, Xue GP, Sprague SJ et al (2007) MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–2245. doi:10.1105/tpc.106.048017
Gigolashvili T, Berger B, Mock HP et al (2007a) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901. doi:10.1111/j.1365-313X.2007.03099.x
Gigolashvili T, Yatusevich R, Berger B et al (2007b) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51:247–261. doi:10.1111/j.1365-313X.2007.03133.x
Gigolashvili T, Engqvist M, Yatusevich R et al (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
Glawischnig E (2007) Camalexin. Phytochemistry 68:401–406. doi:10.1016/j.phytochem.2006.12.005
Glawischnig E, Hansen BG, Olsen CE et al (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc Natl Acad Sci USA 101:8245–8250. doi:10.1073/pnas.0305876101
Grubb CD, Abel S (2006) Glucosinolate metabolism and its control. Trends Plant Sci 11:89–100. doi:10.1016/j.tplants.2005.12.006
Grubb CD, Zipp BJ, Ludwig-Muller J et al (2004) Arabidopsis glucosyltransferase UGT74B1 functions in glucosinolate biosynthesis and auxin homeostasis. Plant J 40:893–908. doi:10.1111/j.1365-313X.2004.02261.x
Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57:303–333. doi:10.1146/annurev.arplant.57.032905.105228
Hansen CH, Du L, Naur P et al (2001a) CYP83B1 is the oxime-metabolizing enzyme in the glucosinolate pathway in Arabidopsis. J Biol Chem 276:24790–24796. doi:10.1074/jbc.M102637200
Hansen CH, Wittstock U, Olsen CE et al (2001b) Cytochrome p450 CYP79F1 from arabidopsis catalyzes the conversion of dihomomethionine and trihomomethionine to the corresponding aldoximes in the biosynthesis of aliphatic glucosinolates. J Biol Chem 276:11078–11085. doi:10.1074/jbc.M010123200
Hemm M, Ruegger M, Chapple C (2003) The Arabidopsis ref2 mutant is defective in the gene encoding CYP83A1 and shows both phenylpropanoid and glucosinolate phenotypes. Plant Cell 15:179–194. doi:10.1105/tpc.006544
Hirai MY, Klein M, Fujikawa Y et al (2005) Elucidation of gene-to-gene and metabolite-to-gene networks in arabidopsis by integration of metabolomics and transcriptomics. J Biol Chem 280:25590–25595. doi:10.1074/jbc.M502332200
Hirai MY, Sugiyama K, Sawada Y et al (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci USA 104:6478–6483. doi:10.1073/pnas.0611629104
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 USA 97:2379–2384. doi:10.1073/pnas.040569997
Jorgensen K, Rasmussen AV, Morant M et al (2005) Metabolon formation and metabolic channeling in the biosynthesis of plant natural products. Curr Opin Plant Biol 8:280–291. doi:10.1016/j.pbi.2005.03.014
Kim JH, Jander G (2007) Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate. Plant J 49:1008–1019
Kim JH, Lee BW, Schroeder F et al (2008) Identification of indole glucosinolate breakdown products with antifeedant effects on Myzus persicae (green peach aphid). Plant J 54:1015–1026
King JJ, Stimart DP, Fisher RH et al (1995) A mutation altering auxin homeostasis and plant morphology in Arabidopsis. Plant Cell 7:2023–2037
Klein M, Reichelt M, Gershenzon J et al (2006) The three desulfoglucosinolate sulfotransferase proteins in Arabidopsis have different substrate specificities and are differentially expressed. FEBS J 273:122–136. doi:10.1111/j.1742-4658.2005.05048.x
Kliebenstein DJ, Gershenzon J, Mitchell-Olds T (2001) Comparative quantitative trait loci mapping of aliphatic, indolic and benzylic glucosinolate production in Arabidopsis thaliana leaves and seeds. Genetics 159:359–370
Kusnierczyk A, Winge P, Midelfart H et al (2007) Transcriptional responses of Arabidopsis thaliana ecotypes with different glucosinolate profiles after attack by polyphagous Myzus persicae and oligophagous Brevicoryne brassicae. J Exp Bot 58:2537–2552. doi:10.1093/jxb/erm043
Lehman AL, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194. doi:10.1016/S0092-8674(00)81095-8
Levy M, Wang Q, Kaspi R et al (2005) Arabidopsis IQD1, a novel calmodulin-binding nuclear protein, stimulates glucosinolate accumulation and plant defense. Plant J 43:79–96. doi:10.1111/j.1365-313X.2005.02435.x
Ljung K, Hull AK, Kowalczyk M et al (2002) Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol Biol 49:249–272. doi:10.1023/A:1015298812300
Ljung K, Hull AK, Celenza J et al (2005) Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17:1090–1104. doi:10.1105/tpc.104.029272
Maruyama-Nakashita A, Nakamura Y, Tohge T et al (2006) Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 18:3235–3251. doi:10.1105/tpc.106.046458
Mewis I, Tokuhisa JG, Schultz JC et al (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 67:2450–2462. doi:10.1016/j.phytochem.2006.09.004
Mikkelsen MD, Hansen CH, Wittstock U et al (2000) Cytochrome P450 CYP79B2 from Arabidopsis catalyzes the conversion of tryptophan to indole-3-acetaldoxime, a precursor of indole glucosinolates and indole-3-acetic acid. J Biol Chem 275:33712–33717. doi:10.1074/jbc.M001667200
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 37:770–777. doi:10.1111/j.1365-313X.2004.02002.x
Nafisi M, Goregaoker S, Botanga CJ et al (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19:2039–2052. doi:10.1105/tpc.107.051383
Naur P, Petersen BL, Mikkelsen MD et al (2003) CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis. Plant Physiol 133:63–72. doi:10.1104/pp.102.019240
Niyogi KK, Fink GR (1992) Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell 4:721–733
Niyogi KK, Last RL, Fink GR et al (1993) Suppressors of trp1 fluorescence identify a new arabidopsis gene, TRP4, encoding the anthranilate synthase beta subunit. Plant Cell 5:1011–1027
Normanly J, Slovin JP, Cohen JD (2005) Auxin metabolism. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action!. Kluwer, Dordrecht, The Netherlands, p 36
Pedras MS, Okinyo DP (2008) Remarkable incorporation of the first sulfur containing indole derivative: another piece in the biosynthetic puzzle of crucifer phytoalexins. Org Biomol Chem 6:51–54. doi:10.1039/b714743k
Piotrowski M, Schemenewitz A, Lopukhina A et al (2004) Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure. J Biol Chem 279:50717–50725. doi:10.1074/jbc.M407681200
Reintanz B, Lehnen M, Reichelt M et al (2001) bus, a bushy arabidopsis cyp79f1 knockout mutant with abolished synthesis of short-chain aliphatic glucosinolates. Plant Cell 13:351–367
Skirycz A, Reichelt M, Burow M 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. doi:10.1111/j.1365-313X.2006.02767.x
Smolen G, Bender J (2002) Arabidopsis cytochrome P450 cyp83B1mutations activate the tryptophan biosynthetic pathway. Genetics 160:323–332
Smolen GA, Pawlowski L, Wilensky SE et al (2002) Dominant alleles of the basic helix-loop-helix transcription factor ATR2 activate stress-responsive genes in Arabidopsis. Genetics 161:1235–1246
Sonderby IE, Hansen BG, Bjarnholt N et al (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. doi:10.1371/journal.pone.0001322
Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4:447–456. doi:10.1016/S1369-5266(00)00199-0
Tantikanjana T, Yong JW, Letham DS et al (2001) Control of axillary bud initiation and shoot architecture in Arabidopsis through the SUPERSHOOT gene. Genes Dev 15:1577–1588. doi:10.1101/gad.887301
Tantikanjana T, Mikkelsen MD, Hussain M et al (2004) Functional analysis of the tandem-duplicated P450 genes SPS/BUS/CYP79F1 and CYP79F2 in glucosinolate biosynthesis and plant development by Ds transposition-generated double mutants. Plant Physiol 135:840–848. doi:10.1104/pp.104.040113
Winkel BS (2004) Metabolic channeling in plants. Annu Rev Plant Biol 55:85–107. doi:10.1146/annurev.arplant.55.031903.141714
Wittstock U, Halkier BA (2000) Cytochrome P450 CYP79A2 from Arabidopsis thaliana L. catalyzes the conversion of l-phenylalanine to phenylacetaldoxime in the biosynthesis of benzylglucosinolate. J Biol Chem 275:14659–14666. doi:10.1074/jbc.275.19.14659
Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (Lond) 95:707–735. doi:10.1093/aob/mci083
Wright AD, Moehlenkamp CA, Perrot GH et al (1992) The maize auxotrophic mutant orange pericarp is defective in duplicate genes for tryptophan synthase beta. Plant Cell 4:711–719
Zhao J, Last RL (1995) Immunological characterization and chloroplast localization of the tryptophan biosynthetic enzymes of the flowering plant Arabidopsis thaliana. J Biol Chem 270:6081–6087. doi:10.1074/jbc.270.11.6081
Zhao J, Williams CC, Last RL (1998) Induction of Arabidopsis tryptophan pathway enzymes and camalexin by amino acid starvation, oxidative stress, and an abiotic elicitor. Plant Cell 10:359–370
Zhao Y, Christensen SK, Fankhauser C et al (2001) A role for flavin monooxygenase-like enzymes in auxin biosynthesis. Science 291:306–309. doi:10.1126/science.291.5502.306
Zhao Y, Hull AK, Gupta NR et al (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112. doi:10.1101/gad.1035402
Acknowledgments
Glucosinolate research in the Bender and Celenza labs is supported by the National Science Foundation grants MCB-0517358 (J. B.) and MCB-0517506 (J.L.C.).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bender, J., Celenza, J.L. Indolic glucosinolates at the crossroads of tryptophan metabolism. Phytochem Rev 8, 25–37 (2009). https://doi.org/10.1007/s11101-008-9111-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-008-9111-7