Light dominates the diurnal emissions of herbivore-induced volatiles in wild tobacco

Jun He,Ian T Baldwin,Meredith C Schuman,Rayko Halitschke

doi:10.1186/s12870-021-03179-z

Abstract

BackgroundTiming is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is particularly relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. Previous studies of the wild tobacco N. attenuata have found associations between the diurnal timing of volatile emissions, and daytime predation of herbivores by their natural enemies.ResultsHere, we investigated the role of light in regulating two biosynthetic groups of volatiles, terpenoids and green leaf volatiles (GLVs), which dominate the herbivore-induced bouquet of N. attenuata. Light deprivation strongly suppressed terpenoid emissions while enhancing GLV emissions, albeit with a time lag. Silencing the expression of photoreceptor genes did not alter terpenoid emission rhythms, but silencing expression of the phytochrome gene, NaPhyB1, disordered the emission of the GLV (Z)-3-hexenyl acetate. External abscisic acid (ABA) treatments increased stomatal resistance, but did not truncate the emission of terpenoid volatiles (recovered in the headspace). However, ABA treatment enhanced GLV emissions and leaf internal pools (recovered from tissue), and reduced internal linalool pools. In contrast to the pattern of diurnal terpenoid emissions and nocturnal GLV emissions, transcripts of herbivore-induced plant volatile (HIPV) biosynthetic genes peaked during the day. The promotor regions of these genes were populated with various cis-acting regulatory elements involved in light-, stress-, phytohormone- and circadian regulation.ConclusionsThis research provides insights into the complexity of the mechanisms involved in the regulation of HIPV bouquets, a mechanistic complexity which rivals the functional complexity of HIPVs, which includes repelling herbivores, calling for body guards, and attracting pollinators.

Highlights

Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds
The genes involved in terpenoid and Green leaf volatiles (GLV) biosynthesis all showed diurnal patterns of transcript accumulation, and the promoter regions of these genes were populated by various cis-acting regulatory elements involved in light, stress, phytohormoneor circadian-regulated processes
But increased GLV emissions Predation assays performed with a biparential RIL population of N. attenuata plants grown in a field plot in the summer of 2017 revealed that M. sexta eggs and larvae were predated by big-eyed bugs (Geocoris spp.) during the day time (Fig. S1), consistent with previous findings [27]

Summary

Introduction

Timing is everything when it comes to the fitness outcome of a plant’s ecological interactions, and accurate timing is relevant for interactions with herbivores or mutualists that are based on ephemeral emissions of volatile organic compounds. He et al BMC Plant Biology (2021) 21:401 predators of herbivores and to indirectly defend themselves from herbivory. Herbivores can use these volatiles to locate their host plants or avoid predation [7, 8]. Terpenoid volatiles are derived from mevalonate (MVA) or the 2-C-methyl-D-erythritol 4-phosphate/ 1deoxy-D-xylulose 5-phosphate (MEP/DOXP) pathway in higher plants [16], and directly synthesized by terpene synthases [15]. Both GLVs and terpenoids play roles in tri-trophic interactions, some of which function as indirect defenses for plants [7, 8]

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Conclusion