The Glucosinolate Biosynthetic Gene AOP2 Mediates Feed-back Regulation of Jasmonic Acid Signaling in Arabidopsis

Molecular Plant

Volumn 8, Issue 8, 2015, Pages 1201-1212

  Burow, Meike ^a   Atwell, Susanna ^b   Francisco, Marta ^b,c   Kerwin, Rachel E ^b   Halkier, Barbara A ^a   Kliebenstein, Daniel J ^a,b  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MISIÓN BIOLÓGICA DE GALICIA CSIC   (Spain)

Author keywords

Arabidopsis; feed back regulation; glucosinolates; JA signaling; jasmonates

Indexed keywords

ARABIDOPSIS;

AOP2 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CYCLOPENTANE DERIVATIVE; GCN5 PROTEIN, ARABIDOPSIS; GLUCOSINOLATE; HISTONE ACETYLTRANSFERASE; JASMONIC ACID; MESSENGER RNA; MYB29 PROTEIN, ARABIDOPSIS; OXYLIPIN; TRANSCRIPTION FACTOR;

ANALYSIS OF VARIANCE; ARABIDOPSIS; BIOLOGICAL MODEL; BIOSYNTHESIS; FEEDBACK SYSTEM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT GENE; PLANT ROOT; SEEDLING; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYCLOPENTANES; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSINOLATES; HISTONE ACETYLTRANSFERASES; MODELS, BIOLOGICAL; OXYLIPINS; PLANT ROOTS; RNA, MESSENGER; SEEDLINGS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84938748490     PISSN: 16742052     EISSN: 17529867     Source Type: Journal    
DOI: 10.1016/j.molp.2015.03.001     Document Type: Article

References (83)

1. S. Anders, P.T. Pyl, and W. Huber HTSeq - a Python framework to work with high-throughput sequencing data Bioinformatics 31 2014 166 169
2. S. Bak, F.E. Tax, K.A. Feldmann, D.W. Galbraith, and R. Feyereisen CYP83B1, a cytochrome P450 at the metabolic branch point in auxin and indole glucosinolate biosynthesis in Arabidopsis Plant Cell 13 2001 101 111
3. J. Beekwilder, W. van Leeuwen, N.M. van Dam, M. Bertossi, V. Grandi, L. Mizzi, M. Soloviev, L. Szabados, J.W. Molthoff, B. Schipper, and et al. The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis PLoS One 3 2008 e2068
4. M. Bekaert, P.P. Edger, C.M. Hudson, J.C. Pires, and G.C. Conant Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis New Phytol. 196 2012 596 605
5. M.G. Bidart-Bouzat, and D. Kliebenstein Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana J. Chem. Ecol. 34 2008 1026 1037
6. N.D. Bonawitz, J.I. Kim, Y. Tobimatsu, P.N. Ciesielski, N.A. Anderson, E. Ximenes, J. Maeda, J. Ralph, B.S. Donohoe, M. Ladisch, and et al. Disruption of Mediator rescues the stunted growth of a lignin-deficient Arabidopsis mutant Nature 509 2014 376 380
7. G. Brader, É. Tas, and E.T. Palva Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora Plant Physiol. 126 2001 849 860
8. P.D. Brown, J.G. Tokuhisa, M. Reichelt, and J. Gershenzon Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana Phytochemistry 62 2003 471 481
9. M. Burow, A. Losansky, R. Muller, A. Plock, D.J. Kliebenstein, and U. Wittstock The genetic basis of constitutive and herbivore-induced ESP-independent nitrile formation in Arabidopsis Plant Physiol. 149 2009 561 574
10. M. Burow, B.A. Halkier, and D.J. Kliebenstein Regulatory networks of glucosinolates shape Arabidopsis thaliana fitness Curr. Opin. Plant Biol. 13 2010 348 353
11. A. Capella, M. Menossi, P. Arruda, and C. Benedetti COI1 affects myrosinase activity and controls the expression of two flower-specific myrosinase-binding protein homologues in Arabidopsis Planta 213 2001 691 699
12. E.K. Chan, H.C. Rowe, J.A. Corwin, B. Joseph, and D.J. Kliebenstein Combining genome-wide association mapping and transcriptional networks to identify novel genes controlling glucosinolates in Arabidopsis thaliana PLoS Biol. 9 2011 e1001125
13. A. Chauvin, D. Caldelari, J.L. Wolfender, and E.E. Farmer Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals New Phytol. 197 2013 566 575
14. F.S. Chew Biological effects of glucosinolates H.G. Cutler, Biologically Active Natural Products 1988 American Chemical Society Washington DC 155 181
15. A. Chini, S. Fonseca, G. Fernández, B. Adie, J.M. Chico, O. Lorenzo, G. García-Casado, I. López-Vidriero, F.M. Lozano, M.R. Ponce, and et al. The JAZ family of repressors is the missing link in jasmonate signalling Nature 448 2007 666 671
16. J.W. de Kraker, K. Luck, S. Textor, J.G. Tokuhisa, and J. Gershenzon Two Arabidopsis genes (IPMS1 and IPMS2) encode isopropylmalate synthase, the branchpoint step in the biosynthesis of leucine Plant Physiol. 143 2007 970 986
17. B. Dombrecht, G.P. Xue, S.J. Sprague, J.A. Kirkegaard, J.J. Ross, J.B. Reid, G.P. Fitt, N. Sewelam, P.M. Schenk, J.M. Manners, and et al. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis Plant Cell 19 2007 2225 2245
18. K.L. Falk, J.G. Tokuhisa, and J. Gershenzon The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms Plant Biol. 9 2007 573 581
19. H.J. Fiebig, and M. Arens Glucosinolate (HPLC-Methode) - Gemeinschaftsarbeiten der DGF, 128. Mitteilung: Deutsche Einheitsmethoden zur Untersuchung von Fetten, Fettprodukten, Tensiden und verwandten Stoffen, 98. Mitt.: Analyse von Fettrohstoffen XII Lipid/Fett 94 1992 199 203
20. M. Freeman Feedback control of intercellular signalling in development Nature 408 2000 313 319
21. H. Frerigmann, and T. Gigolashvili MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana Mol. Plant 7 2014 814 828
22. H. Frerigmann, B. Berger, and T. Gigolashvili bHLH05 is an interaction partner of MYB51 and a novel regulator of glucosinolate biosynthesis in Arabidopsis Plant Physiol. 166 2014 349 369
23. F. Geu-Flores, M.E. Moldrup, C. Bottcher, C.E. Olsen, D. Scheel, and B.A. Halkier Cytosolic gamma-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis Plant Cell 23 2011 2456 2469
24. A. Giamoustaris, and R. Mithen The effect of modifying the glucosinolate content of leaves of oilseed rape (Brassica napus ssp. oleifera) on its interaction with specialist and generalist pests Ann. Appl. Biol. 126 1995 347 363
25. T. Gigolashvili, B. Berger, H.P. Mock, C. Muller, B. Weisshaar, and U.I. Flugge The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana Plant J. 50 2007 886 901
26. T. Gigolashvili, R. Yatusevich, B. Berger, C. Muller, and U.I. Flugge The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana Plant J. 51 2007 247 261
27. T. Gigolashvili, B. Berger, and U.-I. Flügge Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana Phytochem. Rev. 8 2008 3 13
28. T. Gigolashvili, M. Engqvist, R. Yatusevich, C. Muller, and U.I. Flugge HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana New Phytol. 177 2008 627 642
29. G.A. Grant The ACT domain: a small molecule binding domain and its role as a common regulatory element J. Biol. Chem. 281 2006 33825 33829
30. C.H. Hansen, L. Du, P. Naur, C.E. Olsen, K.B. Axelsen, A.J. Hick, J.A. Pickett, and B.A. Halkier CYP83B1 is the oxime-metabolizing enzyme in the glucosinolate pathway in Arabidopsis J. Biol. Chem. 276 2001 24790 24796
31. M.Y. Hirai, M. Yano, D.B. Goodenowe, S. Kanaya, T. Kimura, M. Awazuhara, M. Arita, T. Fujiwara, and K. Saito Integration of transcriptomics and metabolomics for understanding of global responses to nutritional stresses in Arabidopsis thaliana Proc. Natl. Acad. Sci. USA 101 2004 10205 10210
32. M.Y. Hirai, K. Sugiyama, Y. Sawada, T. Tohge, T. Obayashi, A. Suzuki, R. Araki, N. Sakurai, H. Suzuki, K. Aoki, and et al. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis Proc. Natl. Acad. Sci. USA 104 2007 6478 6483
33. R.J. Hopkins, N.M. van Dam, and J.J. van Loon Role of glucosinolates in insect-plant relationships and multitrophic interactions Annu. Rev. Entomol. 54 2009 57 83
34. S. Huseby, A. Koprivova, B.R. Lee, S. Saha, R. Mithen, A.B. Wold, G.B. Bengtsson, and S. Kopriva Diurnal and light regulation of sulphur assimilation and glucosinolate biosynthesis in Arabidopsis J. Exp. Bot. 64 2013 1039 1048
35. B. Joseph, J.A. Corwin, B. Li, S. Atwell, and D.J. Kliebenstein Cytoplasmic genetic variation and extensive cytonuclear interactions influence natural variation in the metabolome Elife 2 2013 e00776
36. R. Jost, L. Altschmied, E. Bloem, J. Bogs, J. Gershenzon, U. Hähnel, R. Hänsch, T. Hartmann, S. Kopriva, C. Kruse, and et al. Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana Photosyn. Res. 86 2005 491 508
37. K. Kai, H. Takahashi, H. Saga, T. Ogawa, S. Kanaya, and D. Ohta Metabolomic characterization of the possible involvement of a Cytochrome P450, CYP81F4, in the biosynthesis of indolic glucosinolate in Arabidopsis Plant Biotechnol. 28 2011 379 385
38. S. Kandel, V. Sauveplane, V. Compagnon, R. Franke, Y. Millet, L. Schreiber, D. Werck-Reichhart, and F. Pinot Characterization of a methyl jasmonate and wounding-responsive cytochrome P450 of Arabidopsis thaliana catalyzing dicarboxylic fatty acid formation in vitro FEBS J. 274 2007 5116 5127
39. D. Kauss, S. Bischof, S. Steiner, K. Apel, and R. Meskauskiene FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg(++)-branch of this pathway FEBS Lett. 586 2012 211 216
40. K. Kazan, and J.M. Manners MYC2: the master in action Mol. Plant 6 2013 686 703
41. R.E. Kerwin, J.M. Jimenez-Gomez, D. Fulop, S.L. Harmer, J.N. Maloof, and D.J. Kliebenstein Network quantitative trait loci mapping of circadian clock outputs identifies metabolic pathway-to-clock linkages in Arabidopsis Plant Cell 23 2011 471 485
42. J.H. Kim, and G. Jander Myzus persicae (green peach aphid) feeding on Arabidopsis induces the formation of a deterrent indole glucosinolate Plant J. 49 2007 1008 1019
43. D.J. Kliebenstein, J. Kroymann, P. Brown, A. Figuth, D. Pedersen, J. Gershenzon, and T. Mitchell-Olds Genetic control of natural variation in Arabidopsis glucosinolate accumulation Plant Physiol. 126 2001 811 825
44. D.J. Kliebenstein, V.M. Lambrix, M. Reichelt, J. Gershenzon, and T. Mitchell-Olds Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate-dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis Plant Cell 13 2001 681 694
45. D.J. Kliebenstein, A. Figuth, and T. Mitchell-Olds Genetic architecture of plastic methyl jasmonate responses in Arabidopsis thaliana Genetics 161 2002 1685 1696
46. A.J.K. Koo, T.F. Cooke, and G.A. Howe Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine Proc. Natl. Acad. Sci. USA 108 2011 9298 9303
47. R. Kumar, Y. Ichihashi, S. Kimura, D.H. Chitwood, L.R. Headland, J. Peng, J.N. Maloof, and N.R. Sinha A high-throughput method for illumina RNA-Seq library preparation Front. Plant Sci. 3 2012 202
48. R.A. Lankau Specialist and generalist herbivores exert opposing selection on a chemical defense New Phytol. 175 2007 176 184
49. G. Li, and C.F. Quiros In planta side-chain glucosinolate modification in Arabidopsis by introduction of dioxygenase Brassica homolog BoGSL-ALK Theor. Appl. Genet. 106 2003 1116 1121
50. J. Li, B.G. Hansen, J.A. Ober, D.J. Kliebenstein, and B.A. Halkier Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis Plant Physiol. 148 2008 1721 1733
51. B. Li, A. Gaudinier, M. Tang, M. Taylor-Teeples, N.T. Nham, C. Ghaffari, D.S. Benson, M. Steinmann, J.A. Gray, S.M. Brady, and et al. Promoter-based integration in plant defense regulation Plant Physiol. 166 2014 1803 1820
52. G. Lobet, L. Pagès, and X. Draye A novel image-analysis toolbox enabling quantitative analysis of root system architecture Plant Physiol. 157 2011 29 39
53. O. Lorenzo, J.M. Chico, J.J. Sanchez-Serrano, and R. Solano JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis Plant Cell 16 2004 1938 1950
54. R. Mauricio Costs of resistance to natural enemies in field populations of the annual plant Arabidopsis thaliana Am. Nat. 151 1998 20 28
55. I. Mewis, H.M. Appel, A. Hom, R. Raina, and J.C. Schultz Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem-feeding and chewing insects Plant Physiol. 138 2005 1149 1162
56. I. Mewis, J.G. Tokuhisa, J.C. Schultz, H.M. Appel, C. Ulrichs, and J. Gershenzon 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 2006 2450 2462
57. M.D. Mikkelsen, B.L. Petersen, E. Glawischnig, A.B. Jensen, E. Andreasson, and B.A. Halkier Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways Plant Physiol. 131 2003 298 308
58. P. Naur, B.L. Petersen, M.D. Mikkelsen, S. Bak, H. Rasmussen, C.E. Olsen, and B.A. Halkier CYP83A1 and CYP83B1, two nonredundant cytochrome P450 enzymes metabolizing oximes in the biosynthesis of glucosinolates in Arabidopsis Plant Physiol. 133 2003 63 72
59. D. Orrell, S. Ramsey, M. Marelli, J.J. Smith, T.W. Petersen, P.d. Atauri, J.D. Aitchison, and H. Bolouri Feedback control of stochastic noise in the yeast galactose utilization pathway Physica D 217 2006 64 76
60. B. Petersen, S. Chen, C. Hansen, C. Olsen, and B. Halkier Composition and content of glucosinolates in developing Arabidopsis thaliana Planta 214 2002 562 571
61. M. Pfalz, M.D. Mikkelsen, P. Bednarek, C.E. Olsen, B.A. Halkier, and J. Kroymann Metabolic engineering in Nicotiana benthamiana reveals key enzyme functions in Arabidopsis indole glucosinolate modification Plant Cell 23 2011 716 729
62. M. Piotrowski, A. Schemenewitz, A. Lopukhina, A. Muller, T. Janowitz, E.W. Weiler, and C. Oecking Desulfoglucosinolate sulfotransferases from Arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure J. Biol. Chem. 279 2004 50717 50725
63. M. Reichelt, P.D. Brown, B. Schneider, N.J. Oldham, E. Stauber, J. Tokuhisa, D.J. Kliebenstein, T. Mitchell-Olds, and J. Gershenzon Benzoic acid glucosinolate esters and other glucosinolates from Arabidopsis thaliana Phytochemistry 59 2002 663 671
64. M.D. Robinson, D.J. McCarthy, and G.K. Smyth edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Bioinformatics 26 2010 139 140
65. H.C. Rowe, B.G. Hansen, B.A. Halkier, and D.J. Kliebenstein Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome Plant Cell 20 2008 1199 1216
66. P.M. Sanders, P.Y. Lee, C. Biesgen, J.D. Boone, T.P. Beals, E.W. Weiler, and R.B. Goldberg The arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway Plant Cell 12 2000 1041 1061
67. F. Schweizer, P. Fernandez-Calvo, M. Zander, M. Diez-Diaz, S. Fonseca, G. Glauser, M.G. Lewsey, J.R. Ecker, R. Solano, and P. Reymond Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior Plant Cell 25 2013 3117 3132
68. A.M. Smith, and M. Stitt Coordination of carbon supply and plant growth Plant Cell Environ. 30 2007 1126 1149
69. I.E. Sønderby, B.G. Hansen, N. Bjarnholt, C. Ticconi, B.A. Halkier, and D.J. Kliebenstein A systems biology approach identifies a R2R3 MYB gene subfamily with distinct and overlapping functions in regulation of aliphatic glucosinolates PLoS One 2 2007 e1322
70. I.E. Sønderby, M. Burow, H.C. Rowe, D.J. Kliebenstein, and B.A. Halkier A complex interplay of three R2R3 MYB transcription factors determines the profile of aliphatic glucosinolates in Arabidopsis Plant Physiol. 153 2010 348 363
71. I.E. Sønderby, F. Geu-Flores, and B.A. Halkier Biosynthesis of glucosinolates-gene discovery and beyond Trends Plant Sci. 15 2010 283 290
72. I. Stenzel, B. Hause, O. Miersch, T. Kurz, H. Maucher, H. Weichert, J. Ziegler, I. Feussner, and C. Wasternack Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana Plant Mol. Biol. 51 2003 895 911
73. N. Stingl, M. Krischke, A. Fekete, and M.J. Mueller Analysis of defense signals in Arabidopsis thaliana leaves by ultra-performance liquid chromatography/tandem mass spectrometry: jasmonates, salicylic acid, abscisic acid Methods Mol. Biol. 1009 2013 103 113
74. A. Stintzi, and J. Browse The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis Proc. Natl. Acad. Sci. USA 97 2000 10625 10630
75. H.U. Stotz, B.R. Pittendrigh, J. Kroymann, K. Weniger, J. Fritsche, A. Bauke, and T. Mitchell-Olds Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of arabidopsis against Egyptian cotton worm but not diamondback moth Plant Physiol. 124 2001 1007 1018 Erratum in Plant Physiol. 125:2203-2203
76. W. Thies Detection and utilization of a glucosinolate sulfohydrolase in the edible snail, Helix pomatia Naturwissenschaften 66 1979 364 365
77. B. Thines, L. Katsir, M. Melotto, Y. Niu, A. Mandaokar, G. Liu, K. Nomura, S.Y. He, G.A. Howe, and J. Browse JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling Nature 448 2007 661 665
78. K.F. Tierens, B.P. Thomma, M. Brouwer, J. Schmidt, K. Kistner, A. Porzel, B. Mauch-Mani, B.P. Cammue, and W.F. Broekaert Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens Plant Physiol. 125 2001 1688 1699
79. C. Trapnell, L. Pachter, and S.L. Salzberg TopHat: discovering splice junctions with RNA-Seq Bioinformatics 25 2009 1105 1111
80. A.M. Wentzell, H.C. Rowe, B.G. Hansen, C. Ticconi, B.A. Halkier, and D.J. Kliebenstein Linking metabolic QTLs with network and cis-eQTLs controlling biosynthetic pathways PLoS Genet. 3 2007 1687 1701
81. T.-M. Yi, Y. Huang, M.I. Simon, and J. Doyle Robust perfect adaptation in bacterial chemotaxis through integral feedback control Proc. Natl. Acad. Sci. USA 97 2000 4649 4653
82. C.L. Zrybko, E.K. Fukuda, and R.T. Rosen Determination of glucosinolates in domestic and wild mustard by high-performance liquid chromatography with confirmation by electrospray mass spectrometry and photodiode-array detection J. Chromatogr. A 767 1997 43 52
83. T. Zust, B. Joseph, K.K. Shimizu, D.J. Kliebenstein, and L.A. Turnbull Using knockout mutants to reveal the growth costs of defensive traits Proc. Biol. Sci. 278 2011 2598 2603