Herbivorous Caterpillars Can Utilize Three Mechanisms to Alter Green Leaf Volatile Emission

Abstract

Green plants emit green leaf volatiles (GLVs) as a general damage response. These compounds act as signals for the emitter plant, neighboring plants, and even for insects in the ecosystem. However, when oral secretions from certain caterpillars are applied to wounded leaves, GLV emissions are significantly decreased or modified. We examined four caterpillar species representing two lepidopteran families for their capacity to decrease GLV emissions from Zea mays leaf tissue. We also investigated the source of the GLV modifying components in the alimentary tract of the various caterpillars. In Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), and Manduca sexta (Linnaeus) (Lepidoptera: Sphingidae), we found three distinct mechanisms to modify GLV emission: a heat-stable compound in the gut, a heat-labile enzyme in salivary gland homogenate (previously described in Bombyx mori (Linnaeus) (Lepidoptera: Bombycidae), and an isomerase in the salivary gland homogenate, which catalyzes the conversion of (Z)-3-hexenal to (E)-2-hexenal (previously described in M. sexta). These mechanisms employed by caterpillars to suppress or modify GLV emission suggest a counteraction against the induced indirect volatile defenses of a plant and provides further insights into the ecological functions of GLVs.

Plant Secondary Metabolites as Defenses, Regulators, and Primary Metabolites: The Blurred Functional Trichotomy

“…the production of defense metabolites per se. As herbivores and pathogens may interfere with the production of defense compounds at many levels, including in the final steps of biosynthesis (Jones et al, 2019), integrating them directly into regulatory feedback loops may allow plants to more accurately monitor and adjust defense accumulation. Using secondary metabolites as defense activation readouts may also help plants to optimize synergies between different defenses and to compensate for accidental failures of specific defense pathways.…”

Silencing the alarm: an insect salivary enzyme closes plant stomata and inhibits volatile release

“…Plant stomata might therefore provide a point of manipulation for insect herbivores. Previous work has shown that caterpillars alter HIPVs; however, the specific components that lead to these modulations remain mostly unclear and speculative (Jones et al ., 2019). Salivary glucose oxidase (GOX) of the polyphagous caterpillar Helicoverpa zea (feeds on > 100 species of plants; Supporting Information Fig.…”

Variability in the Capacity to Produce Damage-Induced Aldehyde Green Leaf Volatiles among Different Plant Species Provides Novel Insights into Biosynthetic Diversity

“…This is mainly because those stresses may individually alter the production of GLV. For example, many insect herbivores modulate GLV emissions through factors abundant in their saliva [41][42][43][44]. Furthermore, cold stress will, as long as its ongoing, likely reduce enzyme activities, including those involved in GLV production [46].…”

“…To analyze damage-induced GLV emissions, we homogenized 50-200 mg of leaf tissue from individual plants by following the general method of Reference [41] with a few modifications. Tissue (excluding the midvein) was cut from fresh leaves and immediately placed in 2-mL screw-cap centrifuge tubes.…”

“…This is of critical importance when performing meaningful experiments with the respective plant, which is always a matter of controversy. Furthermore, in light of recent discoveries on how insect herbivores suppress the production of GLV [41][42][43][44], knowledge about the amounts of GLV that can be produced by the respective plant species is essential in assessing the effectiveness of this suppression. We analyzed the composition of those GLVs with focus on the aldehydes (Z-3-HAL, E-2-HAL, and hexanal), mainly because other GLVs downstream are not produced by damaged tissue since they require intact cells for their biosynthesis [24].…”