Priming of anti‐herbivore defence in Nicotiana attenuata by insect oviposition: herbivore‐specific effects

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 eggprimed 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. sextaoviposited 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.

Nicotiana attenuata's capacity to interact with arbuscular mycorrhiza alters its competitive ability and elicits major changes in the leaf transcriptome

“…We also observed a decline in foliar concentrations of malic acid, rutin and chlorgenic acid in EV plants, while the same compounds also in addition to fraxetin, caffeoylputrescine, scopolin and scopoletin increased in AMF‐inoculated ir CCaMK plants, though not all differences were significant for both inocula. This result at first is surprising as rutin and chlorogenic acid are typically induced by herbivory (Lou and Baldwin ), involved in priming against herbivores (Bandoly et al ) and bacterial pathogens (Yan et al ) and scopolin and scopoletin are known as antifungal compounds (Sun et al ). Moreover, AMF‐inoculated plants are usually considered to be better defended against leaf‐chewing herbivores than non‐colonized plants (Jung et al ).…”

Plant responses to butterfly oviposition partly explain preference–performance relationships on different brassicaceous species

“…Egg-induced plant defense affecting larval performance is especially known for insect species laying eggs in clutches (Hilker and Fatouros 2015). However, plant response to singly laid eggs of Manduca sexta reinforces the defense against M. sexta larvae (Bandoly et al 2016). It remains to be elucidated whether the egg-laying mode (single eggs vs. egg clutches) affects egg-induced plant defense targeting the eggs and how this in turn depends on the plant species receiving the eggs.…”

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

“…Plants on which insects deposited their eggs showed numerous transcriptional changes in response to this highly reliable herbivoreindicating cue (Bonnet et al, 2017;Bruessow, Gouhier-Darimont, Buchala, Metraux, & Reymond, 2010;Firtzlaff, Oberländer, Geiselhardt, Hilker, & Kunze, 2016;Little, Gouhier-Darimont, Bruessow, & Reymond, 2007;Reymond, 2013). Furthermore, plants on which eggs had previously been deposited-such as Arabidopsis, tomato and tobacco plants-showed a stronger induction of defencerelated genes upon damage by feeding larvae (Bandoly, Grichnik, Hilker, & Steppuhn, 2016;Bandoly, Hilker, & Steppuhn, 2015;Kim, Tooker, Luthe, De Moraes, & Felton, 2012;Lortzing et al, 2018). The studies available so far suggest that the egg-mediated, enhanced efficiency of feeding-induced direct defence against insect larvae is linked to changes in phytohormone levels (Kim et al, 2012;Lortzing et al, 2018), increased activity of proteinase inhibitors (Bandoly et al, 2015) and to increased levels of leaf phenylpropanoid derivatives taken up by the larvae (Austel, Eilers, Meiners, & Hilker, 2016;Bandoly et al, 2015Bandoly et al, , 2016Lortzing et al, 2018).…”