Priming of pine defence against insect infestation
Final Report Abstract
Plant stress responses are known to be primable and improved after previous perception of stress indicating (‘warning’) cues. Such priming of stress responses has been shown in particular for angiosperm plants, but also for Scots pine (Pinus sylvestris). This pine species responds to egg deposition by the pine sawfly Diprion pini on its needles by improving the defences against the herbivorous sawfly larvae. Furthermore, Scots pine primed (‘warned’) by exposure to the sawfly’s sex pheromones is known to defend itself more efficiently against D. pini eggs than pine without prior pheromone exposure. The aim of this project was to gain deeper insight into the mechanisms of egg-mediated priming of P. sylvestris defences against D. pini larvae and pheromone-mediated priming of pine defences against D. pini eggs. Our studies of egg-infested pine revealed that the transcriptomic responses of these trees to feeding larvae were weaker than those of trees without eggs. In contrast, the feeding-induced transcriptomic responses of angiosperm plants infested with eggs are known to be stronger than those of egg-free angiosperms, at least in the beginning of larval feeding. However, egginfested, feeding-damaged pine showed similar phytohormonal responses to the infestation as angiosperms. Upon feeding damage, levels of salicylic acid were significantly higher in previously egg-infested pine than in untreated control pine, whereas this was not the case in eggfree, feeding-damaged pine. While salicylic acid and jasmonic acid are usually thought to act antagonistically in anti-herbivore defence, this paradigm does not fit with the phytohormonal changes that occur during egg-mediated priming of plant defences against larval feeding. Our further studies revealed that the priming effect of pine by D. pini sex pheromones is apparently restricted to priming of direct defences against D. pini eggs. No evidence was found that exposure of pine to pheromones affects the indirect, parasitoid-attracting defences against sawfly eggs. Egg deposition by D. pini is known to induce a change in pine odour that is crucial for attraction of egg parasitoids, a finding that was confirmed in our project. However, exposure of pine to the pheromones did not induce a change in the emission of pine needle volatiles, neither in egg-free nor in previously egg-infested pine. Furthermore, the known priming effect that exposure of pine to sawfly sex pheromones exerts on pine direct defences against the eggs did not extend to defences against sawfly larvae. Larvae developed equally well on pheromone-exposed and unexposed trees. The egg-mediated priming of pine defences against sawfly larvae and the pheromone-mediated priming of direct defence against sawfly eggs might render further priming effects of pine due to pheromone exposure redundant. The project opened a previously unforeseen, new question of how the age of pine needles (current-year, previous-year) affects the interactions between the tree and the herbivore. Our investigations showed that D. pini females avoided egg depositions on young (current-year) needles, where the larvae performed worse than on old (previous-year) needles. These results indicate counter-adaptations of D. pini to pine defences. Future studies are needed to further elucidate the role of needle age in shaping (priming of) pine defences against insect infestation.
Publications
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Early herbivore alert: Plant defences against insect eggs. International Congress of Entomology, Helsinki (lecture)
Hilker M.
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Pine defense against eggs of an herbivorous sawfly is elicited by an annexin‐like protein present in egg‐associated secretion. Plant, Cell & Environment, 45(4), 1033-1048.
Hundacker, Janik; Bittner, Norbert; Weise, Christoph; Bröhan, Gunnar; Varama, Martti & Hilker, Monika
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Responses to larval herbivory in the phenylpropanoid pathway of Ulmus minor are boosted by prior insect egg deposition. Planta, 255(1).
Schott, Johanna; Fuchs, Benjamin; Böttcher, Christoph & Hilker, Monika
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Early herbivore alert: Plant defences against insect eggs. IOBC-WPRS PR-IR 2022: “Priming the Future for Healthy Plants”, Univ. Sheffield (lecture)
Hilker, M.
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Priming of Arabidopsis resistance to herbivory by insect egg deposition depends on the plant’s developmental stage. Journal of Experimental Botany, 73(14), 4996-5015.
Valsamakis, Georgios; Bittner, Norbert; Kunze, Reinhard; Hilker, Monika & Lortzing, Vivien
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Adaptive Plasticity of Insect Eggs in Response to Environmental Challenges. Annual Review of Entomology, 68(1), 451-469.
Hilker, Monika; Salem, Hassan & Fatouros, Nina E.
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Early herbivore alert: Plant responses to insect eggs. Leibniz Institute of Vegetable and Ornamental Crops, Großbeeren, Germany (lecture, seminar)
Hilker, M.
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Elm tree defences against a specialist herbivore are moderately primed by an infestation in the previous season. Tree Physiology, 43(7), 1218-1232.
Schott, Johanna; Jantzen, Friederike & Hilker, Monika
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Butterfly eggs prime anti-herbivore defense in an annual but not perennial Arabidopsis species. Planta, 260(5).
Huve, Maryse A. P.; Bittner, Norbert; Kunze, Reinhard; Hilker, Monika; Remus-Emsermann, Mitja N. P.; Paniagua, Voirol Luis R. & Lortzing, Vivien
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Egg priming of plant anti-herbivore defenses in a warming world: A case study in a Lepidoptera-Brassicaceae system. Symposium Insect – Plant Interactions, Bielefeld, Germany (poster)
Huve, M.A.P., Paniagua Voirol, L.R., Hilker, M., Remus-Emsermann, M.N.P. & Lortzing, V.
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Pine Response to Sawfly Pheromones: Effects on Sawfly’s Oviposition and Larval Growth. Insects, 15(6), 458.
Rahman-Soad, Asifur; Bittner, Norbert & Hilker, Monika
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Pine responses to sawfly pheromones: Effects on pine direct and indirect defenses against pine sawflies. Julius-Kühn Institute for Ecological Chemistry, Plant Analysis and Stored Product Protection (lecture)
Rahman-Soad, A.
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Pine responses to sawfly pheromones: Effects on pine direct and indirect defenses against pine sawflies. Symposium Insect – Plant Interactions, Bielefeld, Germany (poster)
Rahman-Soad, A. & Hilker, M.
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Plant defensive responses to insect eggs are inducible by general egg-associated elicitors. Scientific Reports, 14(1).
Lortzing, Vivien; Valsamakis, Georgios; Jantzen, Friederike; Hundacker, Janik; Paniagua, Voirol Luis R.; Schumacher, Fabian; Kleuser, Burkhard & Hilker, Monika
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Sawfly Sex Pheromones: Analysis of Their Impact on Pine Odor Attractive to Egg Parasitoids. Journal of Chemical Ecology, 50(11), 620-630.
Rahman-Soad, Asifur; Skuras, Ludwig; Reinecke, Andreas; Varama, Martti & Hilker, Monika
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The impact of insect egg deposition on Pinus sylvestris transcriptomic and phytohormonal responses to larval herbivory. Tree Physiology, 44(2).
Hundacker, Janik; Linda, Tom; Hilker, Monika; Lortzing, Vivien & Bittner, Norbert
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Tree responses to insect eggs. Annual Meeting International Society of Chemical Ecology, Prague, Czech Republic (lecture)
Hilker, M.
