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Expression profiling of metabolic genes in response to methyl jasmonate reveals regulation of genes of primary and secondary sulfur-related pathways in Arabidopsis thaliana

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Abstract

The treatment of Arabidopsis thaliana with methyl jasmonate was used to investigate the reaction of 2467 selected genes of primary and secondary metabolism by macroarray hybridization. Hierarchical cluster analysis allowed distinctions to be made between diurnally and methyl jasmonate regulated genes in a time course from 30 min to 24 h. 97 and 64 genes were identified that were up- or down-regulated more than 2–fold by methyl jasmonate, respectively. These genes belong to 18 functional categories of which sulfur-related genes were by far strongest affected. Gene expression and metabolite patterns of sulfur metabolism were analysed in detail, since numerous defense compounds contain oxidized or reduced sulfur. Genes encoding key reactions of sulfate reduction as well as of cysteine, methionine and glutathione synthesis were rapidly up-regulated, but none of the known sulfur-deficiency induced sulfate transporter genes. In addition, increased expression of genes of sulfur-rich defense proteins and of enzymes involved in glucosinolate metabolism was observed. In contrast, profiling of primary and secondary sulfur metabolites revealed only an increase in the indole glucosinolate glucobrassicin upon methyl jasmonate treatment. The observed rapid mRNA changes were thus regulated by a signal independent of the known sulfur deficiency response. These results document for the first time how comprehensively the regulation of sulfur-related genes and plant defense are connected. This interaction is discussed as a new approach to differentiate between supply- and demand-driven regulation of the sulfate assimilation pathway.

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Abbreviations

AOP:

2-oxoglutarate-dependent dioxygenase

AOS:

allene oxide synthase

APR:

adenosinephosphosulfate reductase

APS:

ATP sulfurylase

ESP:

epi-thiospecifier protein

FW:

fresh weight

GSH:

glutathione

GST:

glutathione-S-transferase

MeJA:

methyl jasmonate

OAS:

O-acetylserine

SIR:

sulfite reductase

VSP:

vegetative storage protein

References

  • P Armengaud, R Breitling and A Amtmann, The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136 (2004) 2556-2576

    Article  PubMed  CAS  Google Scholar 

  • RP Bodnaryk, Potent effect of jasmonates on indole glucosinolates in oilseed rape and mustard. Phytochemistry 35 (1994) 301-305

    Article  CAS  Google Scholar 

  • H Bohlmann, A Vignutelli, B Hilpert, O Miersch, C Wasternack and K Apel, Wounding and chemicals induce expression of the Arabidopsis thaliana gene Thi2.1, encoding a fungal defense thionin, via the octadecanoid pathway. FEBS L 437 (1998) 281-286

    Article  CAS  Google Scholar 

  • PD Brown, JG Tokuhisa, M Reichelt and J Gershenzon, Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry 62 (2003) 471-481

    Article  PubMed  CAS  Google Scholar 

  • C Brunold and M Suter, Adenosine 5'-phosphosulphate sulphotransferase. In: P Lea (ed.) Methods in Plant Biochemistry. London: Academic Press (1990) pp. 339-343

    Google Scholar 

  • P Buchner, H Takahashi and M Hawkesford, Plant sulphate transporters: co-ordination of uptake, intracellular and long-distance transport. J Exp Bot 55 (2004) 1765-1773

    Article  PubMed  CAS  Google Scholar 

  • SP Ceccotti, RJ Morris and DL Messick, A global overview of the sulphur situation: industry's background, market trends, and commercial aspects of sulphur fertilizers. In: E Schnug (ed.) Sulphur in Agroecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers (1998) pp. 175-201

    Google Scholar 

  • U Dämmgen, K Walker, L Grünhage and H-J Jäger, The atmospheric sulfur cycle. In: E Schnug (ed.) Sulphur in Agroecosystems. Dordrecht, The Netherlands: Kluwer Academic Publishers (1998) pp. 75-114

    Google Scholar 

  • A Devoto and JG Turner, Jasmonate-regulated Arabidopsis stress signalling network. Physiol Plant 123 (2005) 161-172

    Article  CAS  Google Scholar 

  • KJ Doughty, GA Kiddle, BJ Pye, RM Wallsgrove and JA Pickett, Selective induction of glucosinolates in oilseed rape leaves by methyl jasmonate. Phytochemistry 38 (1995) 347-350

    Article  CAS  Google Scholar 

  • B Dysvik and I Jonassen, J-Express: exploring gene expression data using Java. Bioinformatics 17 (2001) 369-370

    Article  PubMed  CAS  Google Scholar 

  • P-H Dubuis, C Marazzi, E Städler and F Mauch, Sulphur deficiency causes a reduction in antimicrobial potential and leads to increased disease susceptibility of oilseed rape. J Phytopath 153 (2005) 27-36

    Article  CAS  Google Scholar 

  • MB Eisen, PT Spellman, PO Brown and D Botstein, Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95 (1998) 14863-14868

    Article  PubMed  CAS  Google Scholar 

  • C Ellis and JG Turner, The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell 13 (2001) 1025-1033

    Article  PubMed  CAS  Google Scholar 

  • F Garcia-Olmedo, P Rodriguez-Palenzuela, A Molina, JM Alamillo, E Lopez-Solanilla, M Berrocal-Lobo and C Poza-Carrion, Antibiotic activities of peptides, hydrogen peroxide and peroxynitrite in plant defence. FEBS Lett 498 (2001) 219-222

    Article  PubMed  CAS  Google Scholar 

  • J Glazebrook, Genes controlling expression of defense responses in Arabidopsis -2001 status. Curr Opin Plant Biol 4 (2001) 301-308

    Article  PubMed  CAS  Google Scholar 

  • J Glazebrook, W Chen, B Estes, H-S Chang, C Nawrath, J-P Métraux, T Zhu and F Katagiri, Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34 (2003) 217-228

    Article  PubMed  CAS  Google Scholar 

  • E Harada, T Kusano and H Sano, Differential expression of genes encoding enzymes involved in sulfur assimilation pathways in response to wounding and jasmonate in Arabidopsis thaliana. J Plant Physiol 156 (2000) 272-276

    CAS  Google Scholar 

  • Y He, H Fukushige, DF Hildebrand and S Gan, Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128 (2002) 876-884

    Article  PubMed  CAS  Google Scholar 

  • R Hell, R Jost, O Berkowitz and M Wirtz, Molecular and biochemical analysis of the enzymes of cysteine biosynthesis in the plant Arabidopsis thaliana. Amino Acids 22 (2002) 245-257

    Article  PubMed  CAS  Google Scholar 

  • R Hell, Molecular physiology of plant sulfur metabolism. Planta 202 (1997) 138-148

    Article  PubMed  CAS  Google Scholar 

  • R Hell and L Bergmann, γ-Glutamylcysteine synthetase in higher plants: catalytic properties and subcellular localization. Planta 180 (1990) 603-612

    Article  CAS  Google Scholar 

  • MY Hirai, T Fujiwara, M Awazuhara, T Kimura, M Noji and K Saito, Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 33 (2003) 651-663

    Article  PubMed  CAS  Google Scholar 

  • MY Hirai, M Yano, DB 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

    Article  PubMed  CAS  Google Scholar 

  • RA Jefferson, TA Kavanagh and MW Bevan, GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6 (1987) 3901-3907

    PubMed  CAS  Google Scholar 

  • DJ 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

    Article  PubMed  CAS  Google Scholar 

  • H Konishi, K Ishiguro and S Komatsu, A proteomics approach towards understanding blast fungus infection of rice grown under different levels of nitrogen fertilization. Proteomics 1 (2001) 1162-1171

    Article  PubMed  CAS  Google Scholar 

  • A Koprivova, M Suter, R Op Camp den, C Brunold and S Kopriva, Regulation of sulfate metabolism by nitrogen in Arabidopsis. Plant Physiol 122 (2000) 737-746

    Article  PubMed  CAS  Google Scholar 

  • V Lambrix, M Reichelt, T Mitchell-Olds, DJ Kliebenstein and J Gershenzon, The Arabidopsis epithiospecifier protein promotes the hydrolysis of glucosinolates to nitriles and influences Trichoplusia ni herbivory. Plant Cell 13 (2001) 2793-2807

    Article  PubMed  CAS  Google Scholar 

  • AG Lappartient, JJ Vidmar, T Leustek, AD Glass and B Touraine, Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18 (1999) 89-95

    Article  PubMed  CAS  Google Scholar 

  • T Leustek, MN Martin, J-A Bick and JP Davies, Pathways and regulation of sulfur metabolism revealed through molecular studies. Annu Rev Plant Physiol Plant Mol Biol 51 (2000) 141-166

    Article  PubMed  CAS  Google Scholar 

  • DH Long, FN Lee and DO TeBeest, Effect of nitrogen fertilization on disease progress of rice blast on susceptible and resistant cultivars. Plant Disease 84 (2000) 403-409

    Article  Google Scholar 

  • A Maruyama-Nakashita, E Inoue, A Watanabe-Takahashi, T Yamaya and H Takahashi, Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol 132 (2003) 597-605

    Article  PubMed  CAS  Google Scholar 

  • MD Mikkelsen, BL Petersen, E Glawischnig, AB Jensen, E Andreasson and BA Halkier, Modulation of CYP79 genes and glucosinolate profiles in Arabidopsis by defense signaling pathways. Plant Physiol 131 (2003) 298-308

    Article  PubMed  CAS  Google Scholar 

  • T Murashige and F Skoog, A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15 (1962) 473-497

    Article  CAS  Google Scholar 

  • T Newman, FJ Bruijn de, P Green, K Keegstra, H Kende, L McIntosh, J Ohlrogge, N Raikhel, S Somerville, M Tomashow, E Retzel and C Somerville, Genes galore: a summary of methods for accessing results from large-scale partial sequencing of anonymous Arabidopsis cDNA clones. Plant Physiol 106 (1994) 1241-1255

    Article  PubMed  CAS  Google Scholar 

  • V Nikiforova, J Freitag, S Kempa, M Adamik, H Hesse and R Hoefgen, Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J 33 (2003) 633-650

    Article  PubMed  CAS  Google Scholar 

  • IAMA Penninckx, BPHJ Thomma, A Buchala, JP Métraux and WF Broekaert, Concomitant activation of jasmonate and ethylene response pathways is required for induction of a pant defensin gene in Arabidopsis. Plant Cell 10 (1998) 2103-2113

    Article  PubMed  CAS  Google Scholar 

  • CM Pieterse and LC Loon van, Salicylic acid-independent plant defence pathways. Trends Plant Sci 4 (1999) 52-58

    Article  PubMed  Google Scholar 

  • KM Ramonell and S Somerville, The genomics parade of defense responses: to infinity and beyond. Curr Op Plant Biol 5 (2002) 291-294

    Article  CAS  Google Scholar 

  • EE Rogers, J Glazebrook and FM Ausubel, Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol Plant Microbe Interact 9 (1996) 748-757

    PubMed  CAS  Google Scholar 

  • K Saito, Regulation of sulfate transport and synthesis of sulfur-containing amino acids. Curr Opin Plant Biol 3 (2000) 188-195

    PubMed  CAS  Google Scholar 

  • K Saito, Sulfur assimilatory metabolism. The long and smelly road. Plant Physiol 136 (2004) 2443-2450

    Article  PubMed  CAS  Google Scholar 

  • Y Sasaki, D Asamizu, Y Shibata, T Nakamura, K Kaneko, T Awai, M Amagai, C Kuwata, T Tsugane, H Masuda, K-I Shimada, S Takamiya, H Ohta and S Tabata, Monitoring of methyl jasmonate-responsive genes in Arabidopsis by cDNA macroarray: self-activation of jasmonic acid biosynthesis and crosstalk with other phytohormone signalling pathways. DNA Res 8 (2001) 153-161

    Article  PubMed  CAS  Google Scholar 

  • Y Sasaki-Sekimoto, T Obayashi, M Matsuumi, Y Kabayashi, E Asamizu, D Shibata, Y Nakamura, T Masuda, H Shimada, K Takamiya, S Tabata and H Ohta, Monitoring of 12-oxo-phytodienoic acid (OPDA)-induced expression changes in Arabidopsis by cDNA macroarray. In: N Murata (ed.) Advanced Research on Plant Lipids. Dordrecht, The Netherland: Kluwer Academic Publishers (2003) pp. 335-338

    Google Scholar 

  • R Schaffer, J Landgraf, M Accerbi, V Simon, M Larson and E Wisman, Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13 (2001) 113-23

    Article  PubMed  CAS  Google Scholar 

  • M Scheideler, NL Schlaich, K Fellenberg, T Beissbarth, NC Hauser, M Vingron, AJ Slusarenko and JD Hoheisel, Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277 (2002) 10555-10561

    Article  PubMed  CAS  Google Scholar 

  • PM Schenk, K Kazan, I Wilson, JP Anderson, T Richmond, SC Somerville and JM Manners, Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97 (2000) 11655-11660

    Article  PubMed  CAS  Google Scholar 

  • PM Schenk, K Kazan, JM Manners, JP Anderson, RS Simpson, IW Wilson, SC Somerville and DJ Maclean, Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol 132 (2003) 999-1010

    Article  PubMed  CAS  Google Scholar 

  • Schnug E, Haneklaus S, Booth E and Walker KC (1995) Sulphur supply and stress resistance in oilseed rape. Proceedings 9th International Rapeseed Congress, Vol 1, pp 229–231. Cambridge

  • FW Smith, MJ Hawkesford, PM Ealing, DT PJ A Clarkson Vandenberg Belcher and AGS Warrilow, Regulation of expression of a cDNA from barley roots encoding a high-affinity sulphate transporter. Plant J 12 (1997) 875-884

    Article  PubMed  CAS  Google Scholar 

  • M Stitt, RMC Lilley, R Gerhard and HW Heldt, Metabolic levels in specific cells and subcellular compartments of plant leaves. Meth Enzymol 174 (1989) 518-552

    Article  CAS  Google Scholar 

  • H Takahashi, M Yamazaki, N Sasakura, A Watanabe, T Leustek, J Almeida Engler de, G Engler, M Montagu van and K Saito, Regulation of sulfur assimilation in higher plants: a sulfate transporter induced in sulfate-starved roots plays a central role in Arabidopsis thaliana. Proc Natl Acad Sci USA 94 (1997) 11102-11107

    Article  PubMed  CAS  Google Scholar 

  • BPHJ Thomma, K Eggermont, IAMA Penninckx, B Mauch-Mani, R Vogelsang, BPA Cammue and WF Broekaert, Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95 (1998) 15107-15111

    Article  PubMed  CAS  Google Scholar 

  • BPHJ Thomma, I Nelissen, K Eggermont and WF Broekaert, Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19 (1999) 163-171

    Article  PubMed  CAS  Google Scholar 

  • BP Thomma, BP Cammue and K Thevissen, Plant defensins. Planta 216 (2002) 193-202

    Article  PubMed  CAS  Google Scholar 

  • KF Tierens, BP Thomma, M Brouwer, J Schmidt, K Kistner, A Porzel, B Mauch-Mani, BP Cammue and WF Broekaert, Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol 125 (2001) 1688-1699

    Article  PubMed  CAS  Google Scholar 

  • G Tsakraklides, M Martin, R Chalam, MC Tarczynski, A Schmidt and T Leustek, Sulfate reduction is increased in transgenic Arabidopsis thaliana expressing 5'-adenylylsulfate reductase from Pseudomonas aeruginosa. Plant J 32 (2002) 879-889

    Article  PubMed  CAS  Google Scholar 

  • SCM Wees Van, H-S Chang, T Zhu and J Glazebrook, Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132 (2003) 606-617

    Article  PubMed  CAS  Google Scholar 

  • P Vauclare, S Kopriva, D Fell, M Suter, L Sticher, P Ballmoos von, U Krähenbühl, R Op Kamp den and C Brunold, Flux control of sulphate assimilation in Arabidopsis thaliana: adenosine 5'-phosphosulphate reductase is more susceptible than ATP sulphurylase to negative control by thiols. Plant J 31 (2002) 729-740

    Article  PubMed  CAS  Google Scholar 

  • JJ Vidmar, D Zhuo, M Yaeesh Siddiqi, JK Schjoerring, B Touraine and DM Glass, Regulation of high-affinity nitrate transporter genes and high-affinity nitrate influx by nitrogen pools in roots of barley. Plant Physiol 123 (2000) 307-318

    Article  PubMed  CAS  Google Scholar 

  • A Vignutelli, C Wasternack, K Apel and H Bohlmann, Systemic and local induction of an Arabidopsis thionin gene by wounding and pathogens. Plant J 14 (1998) 285-295

    Article  PubMed  CAS  Google Scholar 

  • C Wasternack and B Hause, Jasmonates and octadecanoids: Signals in plant stress responses and development. Prog Nucl Ac Res Mol Biol 72 (2002) 165-221

    CAS  Google Scholar 

  • JS Williams, SA Hall, MJ Hawkesford, MH Beale and RM Cooper, Elemental sulfur and thiol accumulation in tomato and defense against a fungal vascular pathogen. Plant Physiol 128 (2002) 150-159

    Article  PubMed  CAS  Google Scholar 

  • JS Williams and RM Cooper, The oldest fungicide and newest phytoalexin – a reappraisal of the fungitoxicity of elemental sulphur. Plant Pathol 53 (2004) 263-279

    Article  CAS  Google Scholar 

  • M Wirtz and R Hell, Production of cysteine for bacterial and plant biotechnology: application of cysteine feedback-insensitive isoforms of serine acetyltransferase. Amino Acids 24 (2003) 195-203

    PubMed  CAS  Google Scholar 

  • M Wirtz, M Droux and R Hell, O-acetylserine (thiol) lyase: an enigmatic enzyme of plant cysteine biosynthesis revisited in Arabidopsis thaliana. J Exp Bot 55 (2004) 1785-1798

    Article  PubMed  CAS  Google Scholar 

  • U Wittstock and J Gershenzon, Constitutive plant toxins and their role in defense against herbivores and pathogens. Curr Opin Plant Biol 5 (2002) 300-307

    Article  PubMed  CAS  Google Scholar 

  • C Xiang and DJ Oliver, Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10 (1998) 1539-1550

    Article  PubMed  CAS  Google Scholar 

  • L Zhang, NS Cohn and JP Mitchel, Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol 112 (1996) 1111-1117

    PubMed  CAS  Google Scholar 

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Jost, R., Altschmied, L., Bloem, E. 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 . Photosynth Res 86, 491–508 (2005). https://doi.org/10.1007/s11120-005-7386-8

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