Skip to main content
SpringerLink
Log in

Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Two cDNAs encoding geranylgeranyl pyrophosphate (GGPP) synthases from tomato (Lycopersicon esculentum) have been cloned and functionally expressed in Escherichia coli. LeGGPS1 was predominantly expressed in leaf tissue and LeGGPS2 in ripening fruit and flower tissue. LeGGPS1 expression was induced in leaves by spider mite (Tetranychus urticae)-feeding and mechanical wounding in wild type tomato but not in the jasmonic acid (JA)-response mutant def-1 and the salicylic acid (SA)-deficient transgenic NahG line. Furthermore, LeGGPS1 expression could be induced in leaves of wild type tomato plants by JA- or methyl salicylate (MeSA)-treatment. In contrast, expression of LeGGPS2 was not induced in leaves by spider mite-feeding, wounding, JA- or MeSA-treatment. We show that emission of the GGPP-derived volatile terpenoid (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene (TMTT) correlates with expression of LeGGPS1. An exception was MeSA-treatment, which resulted in induction of LeGGPS1 but not in emission of TMTT. We show that there is an additional layer of regulation, because geranyllinalool synthase, catalyzing the first dedicated step in TMTT biosynthesis, was induced by JA but not by MeSA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

GGPP:

Geranylgeranyl pyrophosphate

JA:

Jasmonic acid

SA:

Salicylic acid

MeSA:

Methyl salicylate

TMTT:

(E,E)-4,8,12-Trimethyltrideca-1,3,7,11-tetraene

FPP:

Farnesyl pyrophosphate

GPP:

Geranyl pyrophosphate

IPP:

Isopentenyl pyrophosphate

GL:

Geranyllinalool

DMNT:

4,8-Dimethylnona-1,3,7-triene

References

  • Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037

    Article  PubMed  CAS  Google Scholar 

  • Boland W, Gabler A (1989) Biosynthesis of homoterpenes in higher plants. Helv Chim Acta 72:247–253

    Article  CAS  Google Scholar 

  • Boland W, Gabler A, Gilbert M, Feng ZF (1998) Biosynthesis of C-11 and C-16 homoterpenes in higher plants; Stereochemistry of the C-C-bond cleavage reaction. Tetrahedron 54:14725–14736

    Article  CAS  Google Scholar 

  • Botella-Pavia P, Besumbes O, Phillips MA, Carretero-Paulet L, Boronat A, Rodriguez-Concepcion M (2004) Regulation of carotenoid biosynthesis in plants: evidence for a key role of hydroxymethylbutenyl diphosphate reductase in controlling the supply of plastidial isoprenoid precursors. Plant J 40:188–199

    Article  PubMed  CAS  Google Scholar 

  • Bouvier F, Suire C, d’Harlingue A, Backhaus RA, Camara B (2000) Molecular cloning of geranyl diphosphate synthase and compartmentation of monoterpene synthesis in plant cells. Plant J 24:241–252

    Article  PubMed  CAS  Google Scholar 

  • Bouwmeester HJ, Verstappen FW, Posthumus MA, Dicke M (1999) Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean. The first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiol 121:173–180

    Article  PubMed  CAS  Google Scholar 

  • Brading PA, Hammond-Kosack KE, Parr A, Jones JD (2000) Salicylic acid is not required for Cf-2- and Cf-9-dependent resistance of tomato to Cladosporium fulvum. Plant J 23:305–318

    Article  PubMed  CAS  Google Scholar 

  • Burke C, Croteau R (2002) Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch Biochem Biophys 405:130–136

    Article  PubMed  CAS  Google Scholar 

  • Burke CC, Wildung MR, Croteau R (1999) Geranyl diphosphate synthase: cloning, expression, and characterization of this prenyltransferase as a heterodimer. Proc Natl Acad Sci U S A 96:13062–13067

    Article  PubMed  CAS  Google Scholar 

  • Chandra A, Bhatt RK (1998) Biochemical and physiological response to salicylic acid in relation to the systemic acquired resistance. Photosynthetica 35:255–258

    Article  CAS  Google Scholar 

  • Choi D, Ward BL, Bostock RM (1992) Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell 4:1333–1344

    Article  PubMed  CAS  Google Scholar 

  • De Boer JG, Posthumus MA, Dicke M (2004) Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. J Chem Ecol 30:2215–2230

    Article  PubMed  Google Scholar 

  • Dodd DS, Oehlschlager AC (1992) Synthesis of inhibitors of 2,3-oxidosqualene-lanosterol cyclase: conjugate addition of organocuprates to N-(carbobenzyloxy)-3-carbomethoxy-5,6-dihydro-4-pyridone. J Org Chem 57:2794–2803

    Article  CAS  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300:1005–1016

    Article  PubMed  CAS  Google Scholar 

  • Engprasert S, Taura F, Kawamukai M, Shoyama Y (2004) Molecular cloning and functional expression of geranylgeranyl pyrophosphate synthase from Coleus forskohlii Briq. BMC Plant Biol 4:18

    Article  PubMed  Google Scholar 

  • Farag MA, Fokar M, Abd H, Zhang H, Allen RD, Pare PW (2005) (Z)-3-Hexenol induces defense genes and downstream metabolites in maize. Planta 220:900–909

    Article  PubMed  CAS  Google Scholar 

  • Farag MA, Pare PW (2002) C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554

    Article  PubMed  CAS  Google Scholar 

  • Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol 105:405–413

    PubMed  CAS  Google Scholar 

  • Fray RG, Wallace A, Fraser PD, Valero D, Hedden P, Bramley PM, Grierson D (1995) Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway. Plant J 8:693–701

    Article  CAS  Google Scholar 

  • Glazebrook J, Chen WJ, Estes 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 34:217–228

    Article  PubMed  CAS  Google Scholar 

  • Gotoh T, Bruin J, Sabelis MW, Menken SBJ (1993) Host race formation in Tetranychus urticae: genetic differentiation, host plant preference and mate choice in a tomato and cucumber strain. Entomol Exp Appl 68:171–178

    Article  Google Scholar 

  • Graham JS, Pearce G, Merryweather J, Titani K, Ericsson LH, Ryan CA (1985) Wound-induced proteinase inhibitors from tomato leaves. II. The cDNA-deduced primary structure of pre-inhibitor II. J Biol Chem 260:6561–6564

    PubMed  CAS  Google Scholar 

  • Ha SH, Kim JB, Hwang YS, Lee SW (2003) Molecular characterization of three 3-hydroxy-3-methylglutaryl-CoA reductase genes including pathogen-induced Hmg2 from pepper (Capsicum annuum). Biochim Biophys Acta 1625:253–260

    PubMed  CAS  Google Scholar 

  • Hefner J, Ketchum RE, Croteau R (1998) Cloning and functional expression of a cDNA encoding geranylgeranyl diphosphate synthase from Taxus canadensis and assessment of the role of this prenyltransferase in cells induced for taxol production. Arch Biochem Biophys 360:62–74

    Article  PubMed  CAS  Google Scholar 

  • Hopke J, Donath J, Blechert S, Boland W (1994) Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a beta-glucosidase and jasmonic acid. FEBS Lett 352:146–150

    Article  PubMed  CAS  Google Scholar 

  • Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411–1421

    PubMed  CAS  Google Scholar 

  • Hui D, Iqbal J, Lehmann K, Gase K, Saluz HP, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca sexta (lepidoptera, sphingidae) and its natural host Nicotiana attenuata: V microarray analysis and further characterization of large-scale changes in herbivore-induced mRNAs. Plant Physiol 131:1877–1893

    Article  PubMed  CAS  Google Scholar 

  • Joly A, Edwards PA (1993) Effect of site-directed mutagenesis of conserved aspartate and arginine residues upon farnesyl diphosphate synthase activity. J Biol Chem 268:26983–26989

    PubMed  CAS  Google Scholar 

  • Kainou T, Kawamura K, Tanaka K, Matsuda H, Kawamukai M (1999) Identification of the GGPS1 genes encoding geranylgeranyl diphosphate synthases from mouse and human. Biochim Biophys Acta 1437:333–340

    PubMed  CAS  Google Scholar 

  • Kant MR, Ament K, Sabelis MW, Haring MA, Schuurink RC (2004) Differential timing of spider mite-induced direct and indirect defenses in tomato plants. Plant Physiol 135:483–495

    Article  PubMed  CAS  Google Scholar 

  • Kappers IF, Aharoni A, van Herpen TW, Luckerhoff LL, Dicke M, Bouwmeester HJ (2005) Genetic engineering of terpenoid metabolism attracts bodyguards to Arabidopsis. Science 309:2070–2072

    Article  PubMed  CAS  Google Scholar 

  • Kellogg BA, Poulter CD (1997) Chain elongation in the isoprenoid biosynthetic pathway. Curr Opin Chem Biol 1:570–578

    Article  PubMed  CAS  Google Scholar 

  • Koch T, Krumm T, Jung V, Engelberth J, Boland W (1999) Differential induction of plant volatile biosynthesis in the lima bean by early and late intermediates of the octadecanoid-signaling pathway. Plant Physiol 121:153–162

    Article  PubMed  CAS  Google Scholar 

  • Koike-Takeshita A, Koyama T, Obata S, Ogura K (1995) Molecular cloning and nucleotide sequences of the genes for two essential proteins constituting a novel enzyme system for heptaprenyl diphosphate synthesis. J Biol Chem 270:18396–18400

    Article  PubMed  CAS  Google Scholar 

  • Korth KL, Stermer BA, Bhattacharyya MK, Dixon RA (1997) HMG-CoA reductase gene families that differentially accumulate transcripts in potato tubers are developmentally expressed in floral tissues. Plant Mol Biol 33:545–551

    Article  PubMed  CAS  Google Scholar 

  • Lange BM, Ghassemian M (2003) Genome organization in Arabidopsis thaliana: a survey for genes involved in isoprenoid and chlorophyll metabolism. Plant Mol Biol 51:925–948

    Article  PubMed  CAS  Google Scholar 

  • Li L, Li C, Lee GI, Howe GA (2002) Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. Proc Natl Acad Sci U S A 99:6416–6421

    Article  PubMed  CAS  Google Scholar 

  • Liu CJ, Heinstein P, Chen XY (1999) Expression pattern of genes encoding farnesyl diphosphate synthase and sesquiterpene cyclase in cotton suspension-cultured cells treated with fungal elicitors. Mol Plant Microbe Interact 12:1095–1104

    Article  PubMed  CAS  Google Scholar 

  • Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–1168

    Article  PubMed  Google Scholar 

  • Ogura K, Koyama T (1998) Enzymatic aspects of isoprenoid chain elongation. Chem Rev 98:1263–1276

    Article  PubMed  CAS  Google Scholar 

  • Oh SK, Kim IJ, Shin DH, Yang J, Kang H, Han KH (2000) Cloning, characterization, and hetrologous expression of a functional geranylgeranyl pyrophosphate synthase from sunflower (Helianthus annuus L). J Plant Physiol 157:535–542

    CAS  Google Scholar 

  • Okada K, Saito T, Nakagawa T, Kawamukai M, Kamiya Y (2000) Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in Arabidopsis. Plant Physiol 122:1045–1056

    Article  PubMed  CAS  Google Scholar 

  • Park H, Denbow CJ, Cramer CL (1992) Structure and nucleotide sequence of tomato HMG2 encoding 3-hydroxy-3-methyl-glutaryl coenzyme A reductase. Plant Mol Biol 20:327–331

    Article  PubMed  CAS  Google Scholar 

  • Sabelis MW, Janssen A, Kant MR (2001) Ecology. The enemy of my enemy is my ally. Science 291:2104–2105

    Article  PubMed  CAS  Google Scholar 

  • Salzman RA, Brady JA, Finlayson SA, Buchanan CD, Summer EJ, Sun F, Klein PE, Klein RR, Pratt LH, Cordonnier-Pratt MM, Mullet JE (2005) Transcriptional profiling of sorghum induced by methyl jasmonate, salicylic acid, and aminocyclopropane carboxylic acid reveals cooperative regulation and novel gene responses. Plant Physiol 138:352–368

    Article  PubMed  CAS  Google Scholar 

  • Sandmann G, Misawa N, Wiedemann M, Vittorioso P, Carattoli A, Morelli G, Macino G (1993) Functional identification of al-3 from Neurospora crassa as the gene for geranylgeranyl pyrophosphate synthase by complementation with crt genes, in vitro characterization of the gene product and mutant analysis. J Photochem Photobiol B 18:245–251

    Article  PubMed  CAS  Google Scholar 

  • Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721

    Article  CAS  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Metraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Article  PubMed  CAS  Google Scholar 

  • Tholl D, Kish CM, Orlova I, Sherman D, Gershenzon J, Pichersky E, Dudareva N (2004) Formation of monoterpenes in Antirrhinum majus and Clarkia breweri flowers involves heterodimeric geranyl diphosphate synthases. Plant Cell 16:977–992

    Article  PubMed  CAS  Google Scholar 

  • Tornero P, Gadea J, Conejero V, Vera P (1997) Two PR-1 genes from tomato are differentially regulated and reveal a novel mode of expression for a pathogenesis-related gene during the hypersensitive response and development. Mol Plant Microbe Interact 10:624–634

    Article  PubMed  CAS  Google Scholar 

  • Van Poecke RM, Posthumus MA, Dicke M (2001) Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27:1911–1928

    Article  PubMed  Google Scholar 

  • Verdonk JC, Ric de Vos CH, Verhoeven HA, Haring MA, van Tunen AJ, Schuurink RC (2003) Regulation of floral scent production in petunia revealed by targeted metabolomics. Phytochemistry 62:997–1008

    Article  PubMed  CAS  Google Scholar 

  • Zhu XF, Suzuki K, Saito T, Okada K, Tanaka K, Nakagawa T, Matsuda H, Kawamukai M (1997) Geranylgeranyl pyrophosphate synthase encoded by the newly isolated gene GGPS6 from Arabidopsis thaliana is localized in mitochondria. Plant Mol Biol 35:331–341

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Swammerdam Institute for Life Sciences, Department of Plant Physiology, University of Amsterdam, Kruislaan 318, 1098 SM, Amsterdam, The Netherlands

    Kai Ament, Chris C. Van Schie, Michel A. Haring & Robert C. Schuurink

  2. Plant Research International, Post Office Box 16, 6700 AA, Wageningen, The Netherlands

    Harro J. Bouwmeester

Authors
  1. Kai Ament
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris C. Van Schie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Harro J. Bouwmeester
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michel A. Haring
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert C. Schuurink
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert C. Schuurink.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ament, K., Van Schie, C.C., Bouwmeester, H.J. et al. Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta 224, 1197–1208 (2006). https://doi.org/10.1007/s00425-006-0301-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0301-5

Keywords

Search

Navigation