C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato
The exogenous application of (E)-2-hexenal and other C6 components triggers the emission of local and systemic terpenes in tomato plants. Comparative measurements were made between aldehyde doses applied to the plant and levels naturally released from plants with insect damage.
Introduction
Plants have multiple mechanisms to protect themselves against either mechanical wounding, herbivore damage, dessication, or pathogen attack. Jasmonic acid (JA), its methyl ester, certain amino acid conjugates, Glc esters, and various hydroxylated forms, which are collectively termed jasmonates, occur ubiquitously in all plant species and constitute a major signal in stress-induced gene expression (Wasternak and Parthier, 1997). The role of jasmonates in stress-related signaling has been best characterized with respect to the wound-induced expression of proteinase inhibitor (pin) genes, which protect the plant against digestive Ser proteinases of herbivorous insects (Farmer and Ryan, 1992, Koiwa et al., 1997). In both Arabidopsis and tomato plants, JA-deficient mutants have suppressed levels of proteinase inhibitor (PI) proteins and show greater susceptibility to herbivore damage than wild type parental lines (Howe et al., 1996, McConn et al., 1997).
In addition to the elevation of PI or polyphenol oxidase that directly target herbivore pests, plants can also defend themselves against insect damage indirectly by emitting herbivore-induced volatiles that attract natural enemies of the herbivores. These volatile cues operate in several agricultural species, including cotton (Loughrin et al., 1994, Paré and Tumlinson, 1999), lima bean (Dicke et al., 1990, Takabayashi and Dicke, 1996), and tomato (Dicke et al., 1998). Recent studies have indicated that the octadecanoid pathway with jasmonic acid (JA) as the central component is involved in this ancillary defense response. In cotton, lima bean and tomato plants, exposure to jasmonates results in the production of volatiles that mimic those emitted with spider mite damage (Hopke et al., 1994, Boland et al., 1995, Thaler et al., 1996). Airborne-volatiles released upon herbivore damage may also function as signals for neighboring uninfested plants by activating defense related genes (Farmer and Ryan, 1990, Bruin et al., 1995, Miksch and Boland, 1996, Shulaev et al., 1997, Arimura et al., 2000).
While the emissions of terpenoids, nitrogen containing compounds and salicylic acid derivatives vary among plant species, C6-volatiles produced from the catalytic activity of hydroperoxide lyase (HPL) can be generated in all green tissues (Hatanaka et al., 1987) and are among the earliest components to be released from damaged leaves (Turlings et al., 1995). The biosynthesis of C6-volatiles from an 18 carbon fatty acid precursor involves two enzymatic steps catalyzed by lipoxygenase (LOX) and HPL. Depending upon the degree of saturation of the substrate, HPL produces either (Z)-3-hexenal or hexanal. Alcohol dehydrogenase (ADH) and an isomerization factor (IF) catalyze the synthesis of the other C6-volatiles including (E)-2-hexenal, (E)-2-hexenol, (Z)-3-hexenol and hexenol (Hatanaka, 1993).
When released from the plant, these compounds can trigger responses in neighboring plants, including phytoalexin accumulation in cotton (Zeringue, 1992), lower insect feeding rates in tomato (Hildebrand et al., 1993) and reduced germination frequency in soybean (Gardener et al., 1990). Several of these C6- compounds can also act as antimicrobial agents on their own (Croft et al., 1990). As a signal molecule, exogenous application of (E)-2-hexenal to Arabidopsis seedlings induces a group of genes that closely mimics methyl jasmonate (MeJA) induction as well as triggering the up- regulation of LOX pathway and PAL genes (Arimura et al., 2001). Interestingly (E)-2-hexenal treatment does not induce HMGR-1, the gene that encodes a key regulatory step enzyme involved in isoprenoid biosynthesis (Nicholas and Steven, 1998). The role of (E)-2-hexenal as well as other C6- volatile components in triggering VOC emissions is unclear and the broader biological significance of these compounds is under current investigation (Farmer, 2001).
The role of LOX products in stress-related signaling is best characterized with respect to the wound-induced expression of pin genes in tomato. In tomato, an updated model for defense gene activation proposes that C6-volatiles produced by HPL upon wounding is the first step in the octadecanoid-signaling cascade; these C6-volatiles lead to the production of systemin, a systemic intercellular polypeptide signal, that activates the LOX pathway with JA accumulation known to be involved in the induction of pin genes (Sivasankar et al., 2000).
The aim of this research was to examine the role of C6-aldehydes/alcohols in the emission of plant volatiles and compare this response with activated VOC emissions triggered by insect damage. Owing to the wealth of knowledge of plant insect interactions in tomato, this system is likely to provide a good model for assessing the role of oxylipins in the induction of volatile chemicals. Here we report the activation of volatile emissions from the monoterpene and sesquiterpene pathways by a series of C6-volatiles. The release of volatiles from leaves distal to C6-aldehyde treatment supports the theory that green leaf volatiles activate a systemic signaling cascade triggering volatile emissions in untreated leaves.
Section snippets
Whole plant volatile analysis
To determine how tomato plants exposed to C6-aldehyde compare with herbivore damage in triggering VOC emissions, the more abundantly released terpenes and C6-components (Fig. 1A–C) were analyzed and quantified; C6-aldehyde treatment (E-2-hexenal) was also compared with the known signal defense molecule JA by application of its methyl ester MeJA . Accordingly, the major components which overlap with those previously identified in wounded tomato plants (Andersson et al., 1980, Buttery et al., 1987
Plants, insects and reagents
Tomato plants (Lycopersicon esculentum var. Solar Set) were maintained in an insect free-facility in which temp. was maintained at 29±40 °C with a relative humidity 40±10%. Plants were grown under metal halide and high pressure sodium lamps for a 16-h/8-h light/dark photoperiod with a total light intensity of 700 μmol/m2/s. Plants were grown in 16 -cm diameter pots using Pro-gro potting soil having a controlled release fertilizer Osmocot (Scotts-Sierra Horticulture, Marysville, OH). Six
Acknowledgements
We thank R. Jasoni for statistical advice, the Asgrow Vegetable Seeds company (Gonzales, CA) for donation of Solar Set tomato seeds. We are grateful to J.H. Tumlinson, K. Korth and G.A. Howe for their constructive comments concerning an earlier version of this manuscript. This work was supported by NRI Competitive Grants Program/USDA (Award No. 35320–9378).
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