(E,E)-4,8,12-Trimethyltrideca-1,3,7,11- Tetraene in Tomato Are Dependent on Both Jasmonic Acid and Salicylic Acid Signaling Pathways
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Wageningen University & Research Publications Planta (2006) 224:1197–1208 DOI 10.1007/s00425-006-0301-5 ORIGINAL ARTICLE Induction of a leaf speciWc 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 Kai Ament · Chris C. Van Schie · Harro J. Bouwmeester · Michel A. Haring · Robert C. Schuurink Received: 21 November 2005 / Accepted: 11 April 2006 / Published online: 20 June 2006 © Springer-Verlag 2006 Abstract Two cDNAs encoding geranylgeranyl pyro- of TMTT. We show that there is an additional layer of phosphate (GGPP) synthases from tomato (Lycopers- regulation, because geranyllinalool synthase, catalyz- icon esculentum) have been cloned and functionally ing the Wrst dedicated step in TMTT biosynthesis, was expressed in Escherichia coli. LeGGPS1 was predomi- induced by JA but not by MeSA. nantly expressed in leaf tissue and LeGGPS2 in ripen- ing fruit and Xower tissue. LeGGPS1 expression was Keywords Geranylgeranyl pyrophosphate · Jasmonic induced in leaves by spider mite (Tetranychus urticae)- acid · Lycopersicon · Salicylic acid · Spider mites · feeding and mechanical wounding in wild type tomato Homoterpene but not in the jasmonic acid (JA)-response mutant def- 1 and the salicylic acid (SA)-deWcient transgenic NahG Abbreviations line. Furthermore, LeGGPS1 expression could be GGPP Geranylgeranyl pyrophosphate induced in leaves of wild type tomato plants by JA- or JA Jasmonic acid methyl salicylate (MeSA)-treatment. In contrast, SA Salicylic acid expression of LeGGPS2 was not induced in leaves by MeSA Methyl salicylate spider mite-feeding, wounding, JA- or MeSA-treat- TMTT (E,E)-4,8,12-Trimethyltrideca-1,3,7,11-tetraene ment. We show that emission of the GGPP-derived FPP Farnesyl pyrophosphate volatile terpenoid (E,E)-4,8,12-trimethyltrideca- GPP Geranyl pyrophosphate 1,3,7,11-tetraene (TMTT) correlates with expression of IPP Isopentenyl pyrophosphate LeGGPS1. An exception was MeSA-treatment, which GL Geranyllinalool resulted in induction of LeGGPS1 but not in emission DMNT 4,8-Dimethylnona-1,3,7-triene Introduction Electronic Supplementary Material Supplementary material is available to authorised users in the online version of this article at http://dx.doi.org/10.1007/s00425-006-0301-5. Geranylgeranyl pyrophosphate (GGPP) synthase belongs to a group of short-chain prenyltransferases K. Ament · C. C. Van Schie · M. A. Haring · that also include farnesyl pyrophosphate (FPP) syn- R. C. Schuurink (&) thase and geranyl pyrophosphate (GPP) synthase. Swammerdam Institute for Life Sciences, Department of Plant Physiology, University of Amsterdam, These enzymes are involved in isoprenoid biosynthe- Kruislaan 318, 1098 SM Amsterdam, sis and share high sequence homology (Joly and The Netherlands Edwards 1993). An early step in isoprenoid e-mail: [email protected] biosynthesis, catalyzed by GPP synthase, is the con- H. J. Bouwmeester densation of two C5 molecules, isopentenyl pyro- Plant Research International, Post OYce Box 16, phosphate (IPP) and dimethylallyl pyrophosphate 6700 AA Wageningen, The Netherlands (DMAPP) forming GPP (C10). In plants two 123 1198 Planta (2006) 224:1197–1208 separate pathways exist for the synthesis of these infested plants. This suggests that TMTT can inXuence universal C5 intermediates; the cytosolic mevalonate the foraging behavior of predatory mites. pathway and the plastidial methyl-D-erythritol 4- Emission of TMTT in excised lima bean leaves can phosphate pathway. Addition of two IPP molecules be induced by early intermediates of the jasmonic acid to one DMAPP molecule and the addition of one (JA) biosynthetic pathway, linolenic acid and 12-oxo- IPP molecule to GPP is catalyzed by FPP synthase, phytodienoic acid (Koch et al. 1999). There is evidence resulting in FPP (C15). GGPP synthase catalyzes the that, in tomato, emission of TMTT is dependent on JA. formation of GGPP (C20) by condensation of The tomato mutant def-1, which is deWcient in induced DMAPP with three IPP molecules or by the conden- JA-accumulation after wounding or herbivory (Li et al. sation of GPP with two IPP molecules or FPP with 2002), does not emit TMTT upon spider mite-infesta- one IPP molecule (Burke and Croteau 2002). GGPP tion. However, emission of TMTT can be restored by is the precursor for many diVerent products in plants pre-treating these plants with JA (Ament et al. 2004). like diterpenes, gibberellins, carotenoids, the iso- These results indicate that biosynthesis of TMTT is prenoid side chain of chlorophyll and it is used for regulated by oxylipins. protein prenylation. Based on the genome sequence Induced production of terpenes is often correlated Arabidopsis has 12 putative GGPP synthases (Lange to induced terpene synthase activity. Terpene syn- and Ghassemian 2003). Zhu et al. (1997) and Okada thases generate speciWc products from common ter- et al. (2000) have characterized Wve of them and pene precursors. Regulation at the level of terpene showed that they diVer in expression patterns and synthases allows production of a highly speciWc ter- subcellular localization, making it likely that individ- pene blend. However, there are also some reports on ual GGPP synthases have very speciWc functions and the regulation of genes encoding enzymes that act are regulated accordingly. upstream of terpene synthases, resulting in increased (E,E)-4,8,12-Trimethyltrideca-1,3,7,11-tetraene precursor pools. In cytosolic IPP synthesis, 3- (TMTT) is a diterpene-derived volatile produced by hydroxy-3-methylglutaryl-coenzyme A reductase is many plants in response to herbivory. The biosynthe- upregulated in response to pathogens or pathogen- sis of TMTT has been proposed by Boland and derived elicitors in solanaceous plants like tomato Gäbler (1989). They suggest that TMTT is produced (Park et al. 1992), Korean red pepper (Capsicum ann- by oxidative degradation of geranyllinalool (GL). uum) (Ha et al. 2003) and potato (Solanum tubero- This synthesis parallels the biosynthesis of 4,8-dim- sum) (Choi et al. 1992), but also by insect herbivores ethylnona-1,3,7-triene (DMNT), which is likely in potato (Korth et al. 1997) and Nicotiana attenuata formed by oxidative degradation of the sesquiter- (Hui et al. 2003). Furthermore, Kant et al. (2004) pene (E)-nerolidol (Boland et al. 1998). The diter- have shown that transcription of deoxy-xylulose-5- pene GL is supposedly formed by an uncharacterized phosphate synthase, involved in plastidial IPP synthe- GL synthase from the common diterpene precursor sis, is upregulated in tomato upon spider mite-infesta- GGPP. tion. Downstream, at the level of prenyltransferases Herbivore-induced volatiles can beneWt plants by that precede the action of terpene synthases, little is attracting natural enemies of the attacking herbivore known about regulation of gene expression. FPP syn- (Sabelis et al. 2001). Tomato plants infested with spi- thase, required for sesquiterpene biosynthesis, is der mites emit a blend of volatiles that makes them upregulated by pathogens in Korean red pepper (Ha attractive to predatory mites (Phytoseiulus persimilis), et al. 2003) and cotton (Gossypium hirsutum) (Liu a natural enemy of spider mites. Spider mite-infested et al. 1999) and by insect herbivores in maize (Zea tomato plants emit signiWcantly more TMTT than mays) (Farag et al. 2005). GGPP synthase is induced uninfested tomato plants (Kant et al. 2004). The role of in taxus cell suspensions by methyl jasmonate (Hef- TMTT in the attraction of predatory mites has been ner et al. 1998) and by spider mite-herbivory in investigated with lima bean (Phaseolus lunatus) as tomato (Kant et al. 2004). model system (De Boer et al. 2004). Predatory mites To investigate the regulation of TMTT production prefer the odor source of lima bean infested with spi- in tomato we cloned two GGPP synthases from tomato der mites above that of lima bean infested with beet (LeGGPS1, DQ267902 and LeGGPS2, DQ267903), of armyworm (Spodoptera exigua). Spider mite-infested which LeGGPS1 is proposed to be involved in precur- lima bean emits signiWcantly more TMTT than beet sor biosynthesis for TMTT. We also determined the armyworm-infested lima bean. When TMTT is added role of the phytohormones JA and salicylic acid (SA) to the odor of beet armyworm-infested plants, preda- in regulating LeGGPS1 expression and GL synthase tory mites prefer this odor above that of spider mite- activity, leading to TMTT emission. 123 Planta (2006) 224:1197–1208 1199 Materials and methods min. The headspace (the air around the plant) was sampled during 24 h for 2 consecutive days by trapping Chemicals the outgoing air on 300 mg Tenax TA (Alltech, Deer- Weld, IL, USA) in a 5-mm wide glass tube. The com- TMTT was synthesized by Prof. H. Hiemstra (Depart- plete volatile collection set-up was made from glass ment of synthetic organic chemistry, University of and TeXon and no grease was used. The headspace of Amsterdam, The Netherlands) as described by Dodd spider mite-infested plants was collected on the fourth and Oehlschlager (1992). Purity exceeded 98% as was day of spider mite-infestation. Simultaneously, clean checked by NMR and GC-MS. Geranyllinalool, benzyl plants were enclosed in similar desiccators as control acetate and methyl salicylate (MeSA) were obtained treatment. Volatiles of mechanically wounded plants from Fluka (Buchs, Switzerland) and JA from Duchefa were sampled for 24 h directly after damaging the Biochemicals (Haarlem, the Netherlands). plants. After 24 h of treatment with JA or MeSA, plants were placed in clean desiccators and volatiles Plant material and arthropod rearing were sampled in the subsequent 2 days in 24-h inter- vals. The Tenax tubes were eluted with 2 ml pen- Tomato seedlings [Lycopersicon esculentum Mill cv. Cas- tane:diethylether (4:1, v/v) with 1.8 g of benzyl acetate tlemart, def-1 (Howe and Ryan 1999), cv. Moneymaker as internal standard.