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.
SummaryCaterpillar-induced ethylene emissions play an important role in plant-herbivore interactions. The ethylene burst that ensues after attack exceeds wound-induced ethylene emissions, but the mechanisms responsible remain unknown. Adding larval oral secretions (OS) to wounds mimics this ethylene burst. We demonstrate that fatty acid-amino acid conjugates are the responsible elicitors in Manduca sexta OS, and identify genes that are important in OS-elicited ethylene biosynthesis and perception in the larvae's host, Nicotiana attenuata, by examining the consequences of gene silencing on OS-elicited ethylene emissions, as quantified by photo-acoustic spectroscopy. OS elicitation increased transcript accumulation of ACC synthase (ACS), virus-induced gene silencing of ACS halved the OS-elicited ethylene release, and ACC supplementation to ACSsilenced plants restored ethylene emissions, demonstrating that ACS activity limits the rate of release. Silencing three wound-or OS-elicited ACC oxidase (ACO) genes with an ACO consensus fragment abolished the OS-elicited ethylene release. Virus-induced gene silencing of each ACO individually revealed that only NaACO2a and NaACO3 regulate the OS-elicited ethylene release. Transforming plants with various etr1-1 constructs rendered them differentially 'deaf' to ethylene, and dramatically increased the OS-elicited ethylene burst, largely without regulating the transcripts of biosynthetic genes. The volume of the OS-elicited ethylene 'scream' was proportional to the plant's deafness, as determined by 1-MCP treatments. We conclude that the OS-elicited ethylene burst is tuned by a tag-team of transcriptional responses and ethylene perception. Ethylene signaling is shown to be essential in regulating two traits that are important in the N. attenuata-M. sexta interaction: OS-induced nicotine levels and floral longevity.
SummaryHerbivore attacks induce leaves to emit a speci®c blend of volatiles. Here we show that exposure to Tetranychus urticae-induced volatiles, as well as T. urticae infestation and arti®cial wounding, activates the transcription of the genes involved in the biosynthesis of ethylene [S-adenosylmethionine (SAM) synthetase and 1-aminocyclopropane-1-carboxylic acid oxidase] and a gene involved in the biosynthesis of polyamines from SAM (SAM decarboxylase) in lima bean leaves. Moreover, exposure of leaves to any one of the seven major chemical components of T. urticae-induced volatiles also induces expression of these genes. Furthermore, we found that, when lima bean plants were exposed to T. urticae-induced volatiles, they emitted ethylene. Lima bean plants infested by T. urticae and arti®cially wounded plants also emitted ethylene. Endogenous polyamine levels were not increased in the exposed leaves or the infested leaves, suggesting that polyamine production from SAM was only slightly promoted at the metabolic levels present in the leaves. We found that jasmonate (JA) accumulated in leaves exposed to T. urticae-induced volatiles, and that both JA and salicylate (SA) accumulated in leaves infested by T. urticae. These ®ndings, as well as results of pharmacological analyses, suggest that, in leaves exposed to T. urticae-induced volatiles, ethylene biosynthesis might be regulated by pathways involving JA and the ethylene positive feedback loop. They also suggest that ethylene biosynthesis might be regulated by signaling pathways involving JA, SA and ethylene in T. urticae-infested leaves.
The emission of the tropospheric trace gas acetaldehyde was morning after the light was turned on again. This pattern determined in leaves of 4-month-old poplar trees (Populus significantly correlated with diurnal rhythms of stomatal conductance, photosynthesis, transpiration and with the concen-tremula ×P. alba) grown under controlled environmental contrations of ethanol, the assumed precursor of acetaldehyde, in ditions in a greenhouse. Using a dynamic cuvette system the xylem sap of flooded poplar trees. It may be concluded together with a high sensitivity laser-based photoacoustic dethat under conditions of diminished stomatal conductance, tection unit, rates of acetaldehyde emission were measured acetaldehyde emission declines because its diffusive flux is with the high time resolution of about 15 min. Submergence of the roots resulted in the emission of acetaldehyde by the reduced. Alternatively, reduced transpiration may decrease leaves. The emission increased linearly before reaching more ethanol transport from the roots to the shoots and appreciable amounts of the acetaldehyde precursor ethanol are lacking in or less steady-state values (ca 350 nmol m − 2 min − 1 ; ca 470 ng g − 1 dry weight min − 1 ) after approximately 6 h. Prolonged the leaves. The present results support the view that acetaldeflooding of poplar trees resulted in a clear diurnal rhythm of hyde emitted by the leaves of plants is derived from ethanol produced by alcoholic fermentation in submerged roots and acetaldehyde emission. The emission rates decreased when the transported to the leaves with the transpiration stream.
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