Abstract
Main conclusionElms, which have received insect eggs as a ‘warning’ of larval herbivory, enhance their anti-herbivore defences by accumulating salicylic acid and amplifying phenylpropanoid-related transcriptional and metabolic responses to hatching larvae.Plant responses to insect eggs can result in intensified defences against hatching larvae. In annual plants, this egg-mediated effect is known to be associated with changes in leaf phenylpropanoid levels. However, little is known about how trees—long-living, perennial plants—improve their egg-mediated, anti-herbivore defences. The role of phytohormones and the phenylpropanoid pathway in egg-primed anti-herbivore defences of a tree species has until now been left unexplored. Using targeted and untargeted metabolome analyses we studied how the phenylpropanoid pathway of Ulmus minor responds to egg-laying by the elm leaf beetle and subsequent larval feeding. We found that when compared to untreated leaves, kaempferol and quercetin concentrations increased in feeding-damaged leaves with prior egg deposition, but not in feeding-damaged leaves without eggs. PCR analyses revealed that prior insect egg deposition intensified feeding-induced expression of phenylalanine ammonia lyase (PAL), encoding the gateway enzyme of the phenylpropanoid pathway. Salicylic acid (SA) concentrations were higher in egg-treated, feeding-damaged leaves than in egg-free, feeding-damaged leaves, but SA levels did not increase in response to egg deposition alone—in contrast to observations made of Arabidopsis thaliana. Our results indicate that prior egg deposition induces a SA-mediated response in elms to feeding damage. Furthermore, egg deposition boosts phenylpropanoid biosynthesis in subsequently feeding-damaged leaves by enhanced PAL expression, which results in the accumulation of phenylpropanoid derivatives. As such, the elm tree shows similar, yet distinct, responses to insect eggs and larval feeding as the annual model plant A. thaliana.
Highlights
Trees are a rich food source for many herbivorous insects
Environmental cues priming anti-herbivore defences include the first feeding damage prior to subsequent damage, leaf volatiles emitted by damaged neighbouring plants, and insect egg depositions that warn of impending larval feeding damage (Hilker et al 2016, and references therein)
We addressed the following questions: (1) How does the beetle’s egg deposition affect levels of phytohormones in elm leaves subsequently damaged by larval feeding? For this, we analysed levels of Salicylic acid (SA), jasmonic acid (JA), JAisoleucine (JA-Ile) and abscisic acid (ABA). (2) How do transcript levels of genes involved in the phenylpropanoid pathway change in egg-free and egg-primed leaves after the onset of larval feeding? To address this question, we studied transcript levels of the aforementioned genes encoding enzymes catalysing phenylpropanoid biosynthesis
Summary
Trees are a rich food source for many herbivorous insects. Herbivory may threaten forest ecosystems by massive defoliation and the transmission of serious diseases (Boyd et al 2013). Environmental cues priming anti-herbivore defences include the first feeding damage prior to subsequent damage, leaf volatiles emitted by damaged neighbouring plants, and insect egg depositions that warn of impending larval feeding damage (Hilker et al 2016, and references therein). Trees responding to these cues have been shown to improve their anti-herbivore defences against subsequently occurring insect herbivory (Haukioja 1991; Tscharntke et al 2001; Frost et al 2008; Beyaert et al 2012; Austel et al 2016; Li and Blande 2017)
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