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The impact of insect egg deposition on Pinus sylvestris transcriptomic and phytohormonal responses to larval herbivory

ABSTRACT: Plants activate defensive responses to insect herbivory, but also to the initial step of infestation by many insect species, i.e. the egg deposition. They can even improve their defenses against herbivory by responding to previous insect egg deposition. Molecular analysis of these egg-mediated defenses against herbivory focused so far on angiosperm species. Yet, it is unknown how the transcriptome of a gymnosperm species is responding to insect eggs and subsequent larval feeding. Scots pine (Pinus sylvestris) is known to improve its defenses against herbivorous sawfly larvae when previously having received sawfly eggs. Here, we analyzed the transcriptomic and phytohormonal responses of Scots pine needles to eggs and larvae of the sawfly Diprion pini. Pine showed strong transcriptomic responses to both sawfly eggs and larval feeding. Many of the egg-responsive genes were differentially regulated also in response to feeding damage. Various gene ontology (GO) terms were enriched in both egg-laden and in feeding-damaged pine, among them especially GO terms related to cell wall modification, cell death, and jasmonic acid signaling. In contrast to responses of egg-laden angiosperms to insect feeding, pine laden with sawfly eggs showed an attenuated transcriptomic response to subsequent feeding damage. However, in accordance with angiosperm responses, egg-laden pine responded to feeding damage with high SA levels. Based on the detected considerable overlap of egg- and feeding-responsive pine genes we suggest that the strong egg-induced transcriptomic pine response results in maintained defenses against the feeding larvae, thus allowing pine to "afford" attenuated transcriptomic responses to the feeding damage.

ORGANISM(S): Pinus sylvestris

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PROVIDER: S-BSST1074 | biostudies-other |

REPOSITORIES: biostudies-other

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Project description: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.

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The impact of insect egg deposition on Pinus sylvestris transcriptomic and phytohormonal responses to larval herbivory

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