Abstract

Oviposition by Spodoptera exigua on Nicotiana attenuata primes plant defence against its larvae that consequently suffer reduced performance. To reveal whether this is a general response of tobacco to insect oviposition or species-specific, we investigated whether also Manduca sexta oviposition primes N. attenuata's anti-herbivore defence. The plant response to M. sexta and S. exigua oviposition overlapped in the egg-primed feeding-induced production of the phenylpropanoid caffeoylputrescine. While M. sexta larvae were unaffected in their performance, they showed a novel response to the oviposition-mediated plant changes: a reduced antimicrobial activity in their haemolymph. In a cross-resistance experiment, S. exigua larvae suffered reduced performance on M. sexta-oviposited plants like they did on S. exigua-oviposited plants. The M. sexta oviposition-mediated plant effects on the S. exigua larval performance and on M. sexta larval immunity required expression of the NaMyb8 transcription factor that is governing biosynthesis of phenylpropanoids such as caffeoylputrescine. Thus, NaMyb8-dependent defence traits mediate the effects that oviposition by both lepidopteran species exerts on the plant's anti-herbivore defence. These results suggest that oviposition by lepidopteran species on N. attenuata leaves may generally prime the feeding-induced production of certain plant defence compounds but that different herbivore species show different susceptibility to egg-primed plant effects.

Highlights

  • Plants are under attack by a plethora of different herbivores and defend themselves by multifarious traits that are constitutively expressed or inducible upon herbivore attack (Schoonhoven et al 2005)

  • NaMyb8-dependent defence traits mediate the effects that oviposition by both lepidopteran species exerts on the plant’s anti-herbivore defence. These results suggest that oviposition by lepidopteran species on N. attenuata leaves may generally prime the feeding-induced production of certain plant defence compounds but that different herbivore species show different susceptibility to egg-primed plant effects

  • Four and six days after empty clip cages had been applied to control plants, levels of most of the analysed secondary metabolites and trypsin protease inhibitors (TPIs) activity were still unaffected by prior oviposition (Fig. 1: dashed lines; Supporting Information Table S1)

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Summary

Introduction

Plants are under attack by a plethora of different herbivores and defend themselves by multifarious traits that are constitutively expressed or inducible upon herbivore attack (Schoonhoven et al 2005). The feeding damage itself is one of the best investigated stimuli and is perceived by the plant based on the recognition of molecular patterns that are associated with the damage of plant tissue or the attacking herbivore (Heil, 2009). Molecular patterns of both origins shape the plant response to chewing herbivores. The wounding response is modified by the perception of diverse herbivore-associated molecular patterns (Maffei et al 2012) that often consist of modified plant components or are even products of plant enzymes that become active in the insect’s midgut (Gaquerel et al 2012). By integrating different stimuli associated with a feeding herbivore, plants convey responses that are specific to the attacking herbivore

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