Herbivory elicits changes in green leaf volatile production via jasmonate signaling and the circadian clock

Abstract

The timing of plant volatile emissions is important for a robust indirect defense response. Green leaf volatiles (GLVs) are emitted by plants upon damage but can be suppressed by herbivore-associated elicitors, and the abundance and composition of GLVs vary depending on the timing of herbivore attack. We show that the GLV biosynthetic enzyme HYDROPEROXIDE LYASE (HPL) is transcriptionally regulated by the circadian clock in Nicotiana attenuata. In accordance with transcript abundance of NaHPL, GLV aldehyde pools in intact leaves peaked at night and at subjective night under diurnal and continuous light conditions, respectively. Moreover, although the basal abundance of NaHPL transcripts is upregulated by jasmonate (JA) signaling, JA does not regulate the reduction of NaHPL transcript abundance in damaged leaves by simulated herbivore treatment. Unexpectedly, the plant circadian clock was strongly altered when Manduca sexta larvae fed on N. attenuata, and this was also independent of JA signaling. Lastly, the temporal dynamics of NaHPL transcripts and total GLV emissions were strongly altered by M. sexta larval feeding. Our data suggest that the temporal dynamics of emitted GLV blends result from a combination of damage, JA signaling, herbivore-associated elicitors, and the plant circadian clock.

Stress priming, memory, and signalling in plants

“…For example, scarce knowledge is available on whether the competence for getting primed (primability) is a constant feature throughout lifetime or whether it depends on the developmental stage of a plant or is associated with specific organs or tissues (Bouché, Woods, & Amasino, ; Engelbert & Engelbert, ). In addition, further research addressing the influence of daytime and season on stress priming and memory will provide exciting novel insights (Ezer et al, ; Joo et al, ; Nitschke et al, ). Moreover, it will be a challenge to elucidate the impact of a dynamically changing environment on a plant's memory of a specific stress event.…”

“…Herbivory also affects the rhythmicity of damage‐induced biosynthesis of green leaf volatiles (Joo et al, ). When Manduca sexta larvae were feeding upon tobacco leaves, this treatment altered the host plant's circadian clock, which in turn affected the transcriptional regulation of a gene encoding an enzyme involved in green leaf volatile biosynthesis (Joo et al, ). This novel finding highlights the functional relevance of the circadian clock in this process.…”

“…If their predatory search activities are dependent on certain daytimes, disturbance of the rhythmicity of plant odour emission may impair the success in foraging for prey. Joo et al () propose that the plant's clock is hijacked by herbivore‐associated elicitors during the activation of induced defences.…”

Manipulation of Jasmonate Signaling by Plant Viruses and Their Insect Vectors

“…Several types of volatile organic components (VOCs) can be induced by attacks of pathogens/pests or the direct application of JAs, such as terpenes/terpenoids and green leaf volatiles (GLVs). These inducible volatiles are a vital type of defensive signal in the infested plants [52,56]. Therefore, JAs and JA signaling are critical for plant community resistance to herbivores and pathogens.…”

TOC1 in Nicotiana attenuata regulates efficient allocation of nitrogen to defense metabolites under herbivory stress

“…However, there is little evidence under field conditions for an interactive effect between drought and herbivory; a recent study using 16 soybean genotypes failed to find any interactive effects of drought and herbivory on plant performance (Grinnan et al, 2013). The results of the 15 N-labeling experiment (Figs 3, 4), together with previous work by Joo et al (2018), suggest that the circadian machinery plays a greater role in the metabolic state of the plant preceding and immediately at the beginning of herbivory events, and that herbivory-elicited metabolic reorganization decouples the clock from its normal function under control conditions. The use of inducible promoters (see e.g.…”