Abstract
BackgroundSome plants distinguish mechanical wounding from herbivore attack by recognizing specific constituents of larval oral secretions (OS) which are introduced into plant wounds during feeding. Fatty acid-amino acid conjugates (FACs) are major constituents of Manduca sexta OS and strong elicitors of herbivore-induced defense responses in Nicotiana attenuata plants.ResultsThe metabolism of one of the major FACs in M. sexta OS, N-linolenoyl-glutamic acid (18:3-Glu), was analyzed on N. attenuata wounded leaf surfaces. Between 50 to 70% of the 18:3-Glu in the OS or of synthetic 18:3-Glu were metabolized within 30 seconds of application to leaf wounds. This heat-labile process did not result in free α-linolenic acid (18:3) and glutamate but in the biogenesis of metabolites both more and less polar than 18:3-Glu. Identification of the major modified forms of this FAC showed that they corresponded to 13-hydroxy-18:3-Glu, 13-hydroperoxy-18:3-Glu and 13-oxo-13:2-Glu. The formation of these metabolites occurred on the wounded leaf surface and it was dependent on lipoxygenase (LOX) activity; plants silenced in the expression of NaLOX2 and NaLOX3 genes showed more than 50% reduced rates of 18:3-Glu conversion and accumulated smaller amounts of the oxygenated derivatives compared to wild-type plants. Similar to 18:3-Glu, 13-oxo-13:2-Glu activated the enhanced accumulation of jasmonic acid (JA) in N. attenuata leaves whereas 13-hydroxy-18:3-Glu did not. Moreover, compared to 18:3-Glu elicitation, 13-oxo-13:2-Glu induced the differential emission of two monoterpene volatiles (β-pinene and an unidentified monoterpene) in irlox2 plants.ConclusionsThe metabolism of one of the major elicitors of herbivore-specific responses in N. attenuata plants, 18:3-Glu, results in the formation of oxidized forms of this FAC by a LOX-dependent mechanism. One of these derivatives, 13-oxo-13:2-Glu, is an active elicitor of JA biosynthesis and differential monoterpene emission.
Highlights
Some plants distinguish mechanical wounding from herbivore attack by recognizing specific constituents of larval oral secretions (OS) which are introduced into plant wounds during feeding
N-linolenoyl-glutamate is rapidly metabolized on wounded N. attenuata leaf surfaces To investigate the turnover rate of 18:3-Glu on wounded N. attenuata leaves, 0.17 nmoles of synthetic 18:3-Glu, the amount naturally occurring in 10 μL M. sexta OS [14], were applied onto puncture wounds
The total radioactivity recovered after extraction was ca. 90% of the initial radioactivity applied onto the leaf surface, and the peak areas corresponding to metabolites 1, 2, 3 and to the unmodified 18:3-Glu (Fig. 2a) accounted for ca. 8, 15, 35 and 30% of the recovered radioactivity, respectively
Summary
Some plants distinguish mechanical wounding from herbivore attack by recognizing specific constituents of larval oral secretions (OS) which are introduced into plant wounds during feeding. Interactions between plants and invertebrate herbivores have a long history; the first evidence of plant damage by arthropods dates back 400 m years ago [1]. This timeframe has allowed plants and insects to develop sophisticated mechanisms to recognize one another and respond . Among the insect elicitors of plant defense responses, the first to be isolated was the fatty-acid aminoacid conjugate (FAC) volicitin (17-OH-18:3-Gln), which was found in the OS of Spodoptora exigua (S. exigua) larvae feeding on maize (Zea mays) plants and shown to induce a volatile blend different from that induced by wounding alone [6]. The results indicated that elicitation by different insect-derived components is a plant-species specific process [5]
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