Trichome-derived O -acyl sugars are a first meal for caterpillars that tags them for predation

Abstract

Plant glandular trichomes exude secondary metabolites with defensive functions, but these epidermal protuberances are surprisingly the first meal of Lepidopteran herbivores on Nicotiana attenuata. O-acyl sugars, the most abundant metabolite of glandular trichomes, impart a distinct volatile profile to the body and frass of larvae that feed on them. The headspace composition of Manduca sexta larvae is dominated by the branched chain aliphatic acids hydrolyzed from ingested O-acyl sugars, which waxes and wanes rapidly with trichome ingestion. In native habitats a ground-hunting predator, the omnivorous ant Pogonomyrmex rugosus, but not the big-eyed bug Geocoris spp., use these volatile aliphatic acids to locate their prey.indirect defenses | dangerous body odors

Natural history-driven, plant-mediated RNAi-based study reveals CYP6B46 ’s role in a nicotine-mediated antipredator herbivore defense

“…The prey assessment behavior of this predator indicated that it was deterred by a factor related to the larvae's external surface or its headspace. Recently, we discovered that M. sexta larvae emit branched chain aliphatic acids by hydrolyzing the O-acyl sugars that they acquire from the glandular trichomes of N. attenuata (37); this motivated us to explore how larvae might externalize a fraction of their ingested nicotine. As we were budgeting the nicotine flux through the larvae, we found that CYP-silenced larvae had lower hemolymph-and higher frass-nicotine levels, so we examined the dynamics of nicotine in the hemolymph after switching larvae from or to the foliage of nicotine-containing plants.…”

Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature

“…mortality on hemi-ir LOX2 jumped to 70% in the fourth and semi-final larval instar, this was likely due to predation by whiptail lizards ( Cnemidophorus spp.) which were present on the field plot: these lizards predate late-instar Manduca and are attracted to short-chain fatty-acid volatiles produced by the larvae due to ingestion of acyl sugars in plant trichomes (Stork et al, 2011; Weinhold and Baldwin, 2011).

10.7554/eLife.00007.014Figure 9.Cumulative mortality of Manduca spp.

…”

Leaf trichomes affect caterpillar feeding in an instar-specific manner

“…In Solanum lycopersicum , for example, herbivore movement ruptures glandular trichomes and elicits the expression of JA-mediated defense genes even prior to leaf damage [7]. In the Nicotiana tabacum-Manduca sexta system, glandular trichomes have also been shown to release volatiles following caterpillar damage that are attractive to predators [9]. In contrast, non-glandular trichomes are thought to act primarily as mechanical barriers that restrict herbivore movement and thereby prevent feeding damage [3,10].…”

“…For example, two commonly cultivated species, Solanum lycopersicon (tomato) and Nicotiana tabacum (tobacco), have multiple types of glandular trichomes [7,9,13], whereas the common non-domesticated weeds Solanum elaeagnifolium and Solanum carolinense are devoid of any glandular trichomes, but have a dense mat of non-glandular stellate trichomes [3,5,14], (Figure 1). Here using multiple species from Solanaceae, we examined the effects of trichome type X M. sexta larval instar on feeding initiation.

10.1080/19420889.2018.1486653-F0001Figure 1.(a) Trichome morphology of S. eleaegnifolium.

…”