Moth oviposition shapes the species-specific transcriptional and phytohormonal response of Nicotiana attenuata to larval feeding

Abstract

Oviposition by lepidopteran herbivores on Nicotiana attenuata primes plant defence responses that are induced by the feeding larvae. While oviposition by both the generalist Spodoptera exigua and the specialist Manduca sexta primes the production of defensive phenylpropanoids, their larvae are differentially affected. We investigate here the impact of prior oviposition on the transcriptome and phytohormone levels of plants that were later attacked by larvae to find regulatory signals of this priming. In a full-factorial design, we evaluated the effects of oviposition and herbivory by both species. Oviposition alone had only subtle effects at the transcriptional level. Laval feeding alone induced species-specific plant responses. Larvae of the generalist regulated phytohormones and gene expression stronger than larvae of the specialist. A day after larvae started to feed, we detected no significant alterations of the plant’s response to larval feeding due to prior oviposition by conspecific moths. Yet, oviposition by each of the species profoundly influenced the plant’s transcriptional and phytohormonal response to feeding larvae of the other species. Remarkably, the species-specific plant responses to larval feeding shifted towards the response normally elicited by larvae of the ovipositing species. Thus, plants may already recognise an insect’s identity upon its oviposition.

Arabidopsis, tobacco, nightshade and elm take insect eggs as herbivore alarm and show similar transcriptomic alarm responses

“…Accordingly, plants might use the egg stimulus not only to prepare against impending herbivory in general, but to fine-tune the feeding-induced phenylpropanoid defences according to the specific herbivore they are likely to encounter. This idea is further supported by the finding that N. attenuata exhibits altered transcriptomic responses to feeding by S. exigua and M. sexta when the plant has received the eggs of the respective other herbivore prior to feeding 21 .…”

“…Details of the harvesting and plant growth conditions are described in the respective publications. The newly published data on N. attenuata's response to S. exigua eggs were generated using the same methodology as described in Drok et al 21 . These data originate from a leaf systemic to the egg deposition site; the leaf was harvested one day after oviposition.…”

“…affect the feeding-induced changes of JA and SA levels one day after the onset of feeding by conspecific larvae [19][20][21][22] . Prior oviposition on N. attenuata did, however, result in a stronger transcriptional induction of the JA-responsive transcription factor MYB8 after feeding by larvae of the moths Spodoptera exigua or Manduca sexta 19,20 .…”

Herbivore‐specific plant volatiles prime neighboring plants for nonspecific defense responses

“…Previous studies have reported the induction of defense priming in response to different types of priming cues directly associated with herbivory. This includes priming by HIPVs (Engelberth et al, ; Paschold et al, ), oviposition‐associated elicitors deposited on the oviposition site (Bandoly & Steppuhn, ; Drok, Bandoly, Stelzer, Lortzing, & Steppuhn, ; Pashalidou, Lucas‐Barbosa, van Loon, Dicke, & Fatouros, ), and herbivore‐derived olfactory cues such as sex attractants (Helms, De Moraes, Tooker, & Mescher, ). Many priming studies measured defense responses in HIPV‐exposed neighboring plants after subsequent damage by a conspecific herbivore.…”

“…affecting the chewing herbivore Trirhabda virgata , thus suggesting nonspecific defense priming in this system. On the other hand, there are studies documenting herbivore‐specific induction of defense priming for volatiles or oviposition‐mediated priming of plants (Bandoly, Grichnik, Hilker, & Steppuhn, ; Drok et al, ; Moreira et al, ). In Baccharis salicifolia plants, the reproductive rate of either Uroleucon macolai (specialist aphid) or Aphis gossypii (generalist aphid) was only significantly affected or reduced when emitter and receiver plants were damaged by the same aphid species, thus suggesting herbivore‐specific direct defense priming in receiver plants (Moreira et al, ).…”