Elm leaves ‘warned’ by insect egg deposition reduce survival of hatching larvae by a shift in their quantitative leaf metabolite pattern

Abstract

Plants may take insect eggs on their leaves as a warning of future herbivory and intensify their defence against feeding larvae. Responsible agents are, however, largely unknown, and little knowledge is available on this phenomenon in perennial plants. We investigated how egg deposition affects the anti-herbivore defence of elm against the multivoltine elm leaf beetle. Prior egg deposition caused changes in the quality of feeding-damaged leaves that resulted in increased larval mortality and reduced reproductive capacity of the herbivore by harming especially female larvae. Chemical analyses of primary and secondary leaf metabolites in feeding-damaged, egg-free (F) and feeding-damaged, egg-deposited (EF)-leaves revealed only small differences in concentrations when comparing metabolites singly. However, a pattern-focused analysis showed clearly separable patterns of (F) and (EF)-leaves because of concentration differences in especially nitrogen and phenolics, of which robinin was consumed in greater amounts by larvae on (EF) than on (F)-leaves. Our study shows that insect egg deposition mediates a shift in the quantitative nutritional pattern of feeding-damaged leaves, and thus might limit the herbivore's population growth by reducing the number of especially female herbivores. This may be a strategy that pays off in a long run particularly in perennial plants against multivoltine herbivores.

Transcriptomic basis for reinforcement of elm antiherbivore defence mediated by insect egg deposition

“…A further question is whether an early transcriptomic change can explain an ecological effect that is detectable only several days later. While prior egg deposition on elm leaves mediates an earlier and/or faster, and slightly stronger transcriptomic response to the onset of feeding damage, the ecological effects of prior egg deposition on larvae become evident only in the course of larval development; elm leaf beetle larvae suffer significantly higher mortality only after an 8‐day feeding period, but not earlier (Austel et al., ). We suggest that the differences observed in the dynamics of the transcriptomic response of egg‐free and egg deposition‐treated elm leaves at the beginning of the feeding damage might cause slight differences in the leaf metabolome at later time points in the course of continuous larval feeding.…”

“…The enrichment of elm transcripts from GO categories related to cell wall organization processes and the phenylpropanoid pathway in egg deposition‐treated leaves indicates subsequent changes in cell wall quality and phenylpropanoid patterns. Indeed, the metabolite pattern of egg deposition‐treated and egg‐free leaves has been shown to differ especially with respect to quantities of phenylpropanoid derivatives (among them the flavonoid robinin) after an 8‐day larval feeding period (Austel et al., ). The finding that prior egg deposition results in enhanced levels of phenylpropanoid derivatives in feeding‐induced leaves has also been shown in tobacco plants infested by moth eggs and larvae (Bandoly et al., ; in this case, caffeoylputrescine) and in A. thaliana infested with butterfly eggs and larvae (Lortzing et al., ; kaempferol derivatives).…”

“…This leaf treatment—removal of a small piece of leaf epidermis plus application of the sticky oviduct secretion—has also been used by Austel et al. (), who showed that mimicking egg deposition in this way results in a reinforced defence against elm leaf beetle larvae. Furthermore, this leaf treatment is known to induce a so‐called indirect defence involving egg parasitoids.…”

“…In addition to the above‐mentioned herbaceous plant species, elm trees ( Ulmus minor ) also mount a more efficient defence against herbivory when having received insect egg depositions on their leaves prior to feeding damage. Elm leaf beetle larvae ( Xanthogaleruca luteola ) feeding upon elm leaves which received eggs of this beetle species suffer higher mortality than larvae feeding upon egg‐free leaves (Austel et al., ). A statistical comparison of the metabolite patterns of feeding‐damaged elm leaves with and without prior egg deposition revealed, in particular, differences in the levels of several phenylpropanoids (flavonoids).…”

“…A statistical comparison of the metabolite patterns of feeding‐damaged elm leaves with and without prior egg deposition revealed, in particular, differences in the levels of several phenylpropanoids (flavonoids). Among them, high levels of the phenylpropanoid derivative robinin (= kaempferol‐3‐ O ‐robinoside‐7‐ O ‐rhamnoside, a flavone glycoside) were shown to increase larval mortality; larvae feeding on leaves with previous egg depositions need to cope with enhanced robinin levels (Austel et al., ). Hence, previously egg‐deposited elm leaves can more efficiently limit the abundance of a specialized herbivore due to an egg‐mediated change of the feeding‐induced metabolite pattern.…”