Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore

Abstract

Herbivory induces both direct and indirect defenses in plants; however, some combinations of these defenses may not be compatible. The jasmonate signal cascade activated both direct (nicotine accumulations) and indirect (mono- and sesquiterpene emissions) whole-plant defense responses in the native tobacco Nicotiana attenuata Torr. Ex Wats. Nicotine accumulations were proportional to the amount of leaf wounding and the resulting increases in jasmonic acid (JA) concentrations. However, when larvae of the nicotine-tolerant herbivore, Manduca sexta, fed on plants or their oral secretions were applied to leaf punctures, the normal wound response was dramatically altered, as evidenced by large (4- to 10-fold) increases in the release of (i) volatile terpenoids and (ii) ethylene, (iii) increased (4- to 30-fold) accumulations of endogenous JA pools, but (iv) decreased or unchanged nicotine accumulations. The ethylene release, which was insensitive to inhibitors of induced JA accumulation, was sufficient to account for the attenuated nicotine response. Applications of ethylene and ethephon suppressed the induced nicotine response and pre-treatment of plants with a competitive inhibitor of ethylene receptors, 1-methylcyclopropene, restored the full nicotine response. This ethylene burst, however, did not inhibit the release of volatile terpenoids. Because parasitoids of Manduca larvae are sensitive to the dietary intake of nicotine by their hosts, this ethylene-mediated switching from direct to a putative indirect defense may represent an adaptive tailoring of a plant's defense response.

Plant Senescence: The Role of Volatile Terpene Compounds (VTCs)

“…Using detached lima bean leaves (Phaseoluslunatus L), [71] demonstrated that exogenous applications of the ethylene precursor, 1-aminocyclopropane-1-carboxylic acid, enhance JA-induced VTC emission. However, in tobacco (Nicotiana attenuata), [72] did not detect any significant interactions between exogenous methyl jasmonate and ethylene upon in- Current study contradicts reports of VTC-dependent ethylene senescence or vice versa. In a study to determine the effect of ethylene on VTC synthesis and how their interaction affect postharvest balsam fir needle abscission through the inhibition of ethylene synthesis using aminoethoxyvinylglycine (AVG), it was discovered that although AVG was effective in inhibiting ethylene synthesis and delaying postharvest needle abscission there was no changes in the type and amount of VTCs synthesized compared to the control [15].…”

Absolute Configuration of Volicitin from the Regurgitant of Lepidopteran Caterpillars and Biological Activity of Volicitin-Related Compounds

“…9) Fatty acid-amino acid conjugates in the oral secretions of two Manduca species elicited bursts in the production of jasmonic acid 5) and ethylene. 5,10) These results clearly show that volicitin-related compounds evoked some plant defense responses.…”

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

“…The induced increase in JA levels that are normally proportional to the amount of mechanical wounding erupts into a JA burst that increases concentrations two to 10 times wound-induced levels (McCloud and Kahl et al, 2000;Ziegler et al, 2001) and is propagated throughout the damaged leaf ahead of the rapidly foraging herbivore (Schittko et al, 1999). Wounding and JA-elicitation do not result in ethylene emissions, but tobacco hornworm attack produces a rapid ethylene burst, which is sustained during larval feeding .…”