Plant priming of anti-herbivore defences by insect oviposition

Principal Investigator: Prof. Dr. Anke Steppuhn

Insect oviposition often precedes the attack of plants by herbivorous larvae. Project B2 investigates oviposition-mediated priming of plant defences to future insect herbivory in two solanaceaous plant species. In phase I, we demonstrated that oviposition by generalist and specialist lepidopteran herbivores increases resistance to larval feeding in both plant species. In the annual plant Nicotiana attenuata, we identified feeding-induced defence traits that are primed by preceding oviposition in systemic leaves and revealed that these traits mediate the increased resistance of oviposited plants. In the perennial plant Solanum dulcamara, oviposition locally induces chlorosis, ROS production and neoplasms at the oviposition site. These responses are associated with increased levels of salicylic acid (SA) and expression of genes related to pathogen resistance and a decreased egg survival. In systemic leaves of both plant species, oviposition per se did not alter phytohormone levels or transcript profiles, but the feeding-induced transcriptional reprogramming. Based on this characterisation of oviposition-primed plant responses to herbivory and the ecological effects of the priming by insect eggs, B2 aims to focus in phase II (i) on the regulation of the primed state which remains to be determined.

Oviposition-primed plants of both species suffered reduced feeding damage by at least one of its native herbivores suggesting that the priming of defence responses are beneficial for the plant. Yet, the best evidence for the adaptive value of traits is a fitness benefit of the organism expressing that trait. The benefit of priming over directly inducing plant defence in response to stimuli that reliably predict upcoming herbivory is assumed to lie in the avoidance of production costs in all occasions that the herbivore eggs do not hatch (e.g. due to predation). Therefore, we aim (ii) to scrutinise in phase II the fitness benefits and costs of priming in relation to that of induced plant defence.

The comparative analysis of the plant responses to generalist and specialist lepidopteran herbivores revealed herbivore-specific effects beyond largely overlapping plant responses. Opposite to the other herbivores investigated, the tobacco specialist Manduca sexta did not perform worse on oviposited plants despite a priming of direct defence traits as well as of the feeding-induced plant volatile blend. Feeding-induced volatiles are involved in indirect plant defence via predators, an effective defence strategy against this specialist herbivore that is adapted to tobacco direct defence traits. The results of our studies in phase I indicate that oviposition-mediated effects interact with the function of indirect defences against feeding larvae. In phase II we aim (iii) to further explore this interaction.

Accordingly, the key questions of project B2 during phase II are: (i) How fast is a primed state established and how fast does it cease after removal of the priming stimulus? (ii) How does oviposition affect plant fitness of herbivore-attacked and unattacked plants? (iii) How does insect oviposition affect indirect plant defence against feeding larvae?

References

• Bandoly, M., Hilker, M. and Steppuhn, A. 2015. Oviposition by Spodoptera exigua on Nicotiana attenuata primes induced plant defense against larval herbivory. Plant J. 83: 661-672.
• Bandoly, M., Hilker, M. and Steppuhn, A. 2015. Priming of anti-herbivore defence in Nicotiana attenuata by insect oviposition: Herbivore specific effects. Plant Cell Environm. doi: 10.1111/pce.12677.
• Bandoly, M. and Steppuhn, A. 2015. A push-button: Spodoptera exigua oviposition on Nicotiana attenuata dose-independently primes the feeding-induced plant defence. Plant, Signal Behav. doi: 10.1080/15592324.2015.1114198.
• Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Bäurle, I., Geiselhardt, S., Hincha, D.K., Kunze, R., Mueller-Roeber, B., Rillig, M.C., Rolff, J., Romeis, T., Schmülling, T., Steppuhn, A., van Dongen, J., Withcomb, S.J., Wurst, S., Zuther, E. and Kopka, J. 2015. Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. doi: 10.1111/brv.12215.