Ecophysiological comparison of direct and indirect defenses in Nicotiana attenuata

Abstract

After herbivore attack, plants launch a suite of direct and indirect defense responses that must be coordinated if plants are to realize a fitness benefit from these responses. Here we characterize the volatile emissions in the native tobacco plant, Nicotiana attenuata Torr. ex Wats., that are elicited by tobacco hornworm (Manduca sexta L.) attack and are known to function as attractants for parasitoids. To provide the first ecophysiological comparison of examples of both types of defense in the same species, we characterize the elicitation and signaling mechanisms, the resources required, and the potential costs and benefits of the volatile release and compare these traits with those of the well-described induced direct defense in this species, nicotine production. The release of (E)-β-ocimene, cis-α-bergamotene and linalool is dramatically induced within 24 h by application of methyl jasmonate (MeJA), caterpillar feeding, and the treatment of mechanical wounds with larval oral secretions (OS), but not by mechanical damage alone. Plants from different geographic locations produce volatile blends that differ in composition. The most consistently released component from all genotypes, cis-α-berga-motene, is positively related to the amount of MeJA and the level of wounding if OS are applied to the wounds. The volatile release is strongly light dependent, dropping to undetectable quantities during dark periods, even when temperatures are elevated to match those of the light period. Inhibitors of wound-induced jasmonate accumulation (salicylates and auxins), which are known to inhibit wound-induced nicotine production, do not inhibit the release of volatiles. By individually inducing different leaf positions with OS and, on other plants, excising them after induction, we demonstrate that the emission is largely a systemic, whole-plant response, which is maximally triggered when the second fully expanded leaf is induced. We conclude that while both are whole-plant, systemic responses that utilize recently acquired resources for their production and are activated by the jasmonate cascade, the elicitation of the volatile release exhibits greater tissue sensitivity and utilizes additional signaling components than does nicotine production. In contrast to the large investment of fitness-limiting resources required for induced nicotine production or the resources used in benzyl acetone release from flowers for pollinator attraction, the resource requirements for the volatile release are minor. Hence the argument that the volatile release incurs comparatively large physiological costs cannot be supported in this system.

Exogenous Application of Jasmonic Acid Induces Volatile Emissions in Rice and Enhances Parasitism of Nilaparvata lugens Eggs by theParasitoid Anagrus nilaparvatae

“…As reported for other plants, such as tobacco (Halitschke et al, 2000), maize (Schmelz et al, 2003), and lima bean , wounding and application of JA to rice plants also resulted in an increase in volatiles emitted. The overall emission was almost fourfold higher than the emission of the buffer-treated plants.…”

“…In maize, for example, it has been observed that excised leaves produced a 2.5-to 8.0-fold greater volatile in response to JA and the caterpillar produced elicitor volicitin than similarly treated intact plants (Schmelz et al, 2001). Herbivore-or elicitor-induced volatile releases also vary with time after treatment (Turlings et al, 1998), herbivore damage level (Gouinguene et al, 2003), and the applied elicitor amount (Halitschke et al, 2000). Compared to the nonmanipulated rice plants, wounding and application of the buffer also increased release of some volatiles ( Figure 5), suggesting that wounding alone may be sufficient to induce a minor release of at least some of the compounds and that application of JA fortifies this effect.…”

“…In the wild tobacco plant Nicotiana attenuata, for example, exogenous application of MeJA increases the release of volatile organic compounds (Halitschke et al, 2000), which enhances the mortality rates of the herbivores by attracting the natural enemies of herbivores (Kessler and Baldwin, 2001). Moreover, antisense suppression of a lipoxygenase gene LOX3, a specific wound-and herbivory-induced isoform involved in JA biosynthesis in N. attenuata, results in decreases in release of volatiles and nicotine and trypsin protease inhibitor levels (Halitschke and Baldwin, 2003).…”

Variation of Herbivore-Induced Volatile Terpenes among Arabidopsis Ecotypes Depends on Allelic Differences and Subcellular Targeting of Two Terpene Synthases, TPS02 and TPS03

“…While the variation of herbivore-induced volatiles has been studied in some wild species (Halitschke et al, 2000;Gouinguene et al, 2001;Delphia et al, 2009), knowledge of the molecular mechanisms governing the natural diversity of volatile compounds is rather limited. We have been investigating the intraspecific and interspecific variation of volatile profiles in Arabidopsis species (Tholl et al, 2005;Abel et al, 2009) to explore the natural evolution of volatile mixtures in more detail.…”

An Ecologically Motivated Analysis of Plant-Herbivore Interactions in Native Tobacco

“…JA elicitation and herbivore attack from four different species of insects-but not mechanical wounding-cause plants to systemically release a bouquet of mono-and sesquiterpenes, in addition to the green leaf volatiles that are primarily released from the wounded leaves (Halitschke et al, 2000;Kessler and Baldwin, 2001). This herbivore-induced volatile release occurs principally during the day and cannot be inhibited by treating attacked tissues with lypoxygenase inhibitors (Halitschke et al, 2000). The volatile release has been verified in plants grown in native populations, where it functions as an indirect defense in two distinct ways.…”