Acute toxicity of the plant volatile indole depends on herbivore specialization

Abstract

207 21 Abstract 33Herbivore-induced plant volatiles (HIPVs) provide direct benefits to plants as 34 antimicrobials and herbivore repellents, but their potential as direct toxins to herbivores is 35 unclear. Here we assayed the larvicidal activity of six common HIPVs from three different 36 biochemical pathways and tested the hypothesis that the larvicidal activity of HIPVs is related to 37 the host specialization of the insect pest. We first assessed β-caryophyllene, linalool, z-3-38 hexenyl acetate, z-3-hexenol, e-2-hexenol, and indole against the beet armyworm (Spodoptera 39 exigua), and found that indole was 7-fold more toxic compared to the other volatiles when 40 incorporated into diet. Then, we tested the larvicidal activity of indole against six common, 41 destructive pest caterpillars with varying host ranges. Consistent with our hypothesis, indole 42 toxicity varied with caterpillar host range: indole toxicity was seven-fold higher in more 43 specialized insect species relative to generalist insect species. That said, the LC 50 of indole was 44 comparable to other reported anti-herbivore agents even against the generalist caterpillars. Yet, 45 indole in headspace had neither larvicidal nor ovicidal activity on any caterpillar species tested. 46 These results support a key ecological precept regarding tradeoffs between host specialization 47 49 50 Keywords 51 Caterpillars, Green leaf volatiles (GLVs), Herbivore-induced plant volatiles (HIPVs), Host Range, 52 Indole, Pest, Toxicity, Specialist vs Generalist herbivore 53 54Key message 55 • We measured the direct toxicity of six common HIPVs against the beet armyworm. 56• Indole was the most toxic HIPV against the beet armyworm. 57• We determined the toxicity of indole against six different pest caterpillar species. 58• Toxicity of indole was associated with the host preference of the insect species. 59• Indole exposure in headspace had no effect on egg hatching or caterpillar survival. 60

Tolerance, biochemistry and related gene expression in Pagiophloeus tsushimanus (Coleoptera: Curculionidae) exposed to chemical stress from headspace host‐plant volatiles

“…We used this model since it is generally applied for the description of logistic dose responses in pharmacology and chemistry (Maurya et al, 2020). All quantitative data were tested for normality using the…”

“…Larval survivorship and egg hatchability after 24 h of exposure were regressed against the treatment concentrations using nonlinear regression analysis, and the LC 50 value was calculated using the fitted function: where y and x are response and dose variables, respectively; A 1 and A 2 are initial and final value, respectively; x 0 is centre; and P is power. We used this model since it is generally applied for the description of logistic dose responses in pharmacology and chemistry (Maurya et al, 2020). All quantitative data were tested for normality using the Shapiro–Wilk test and expressed as the mean ± SE values.…”

“…The last several decades have witnessed an increase in the study of plant-derived attractants and their exploitation in integrated pest management (IPM) (Spochacz et al, 2018), including IPM for pest weevils (Kendra et al, 2016(Kendra et al, , 2017. On the other hand, most plant volatiles, as defensive traits, are physiologically toxic to insect pests at high concentrations (Maurya et al, 2020). A classical example is provided by a variety of plant essential oils, which present promise for use as environmentally friendly alternatives to chemical pesticides in agriculture and forest systems (Ebadollahi & Jalali, 2015).…”

Volatile DMNT directly protects plants against Plutella xylostella by disrupting the peritrophic matrix barrier in insect midgut

“…Another major line of plant defense relies on the ability to kill pests directly via the secretion of natural products that are harmful to insects. For instance, various HIPVs including indole have been reported to show direct toxicity to beet armyworm ( Maurya et al, 2020 ). Some maize ( Zea mays L.) ecotypes produce a 33 kDa cysteine protease in response to caterpillar feeding that damages the insect intestine, leading to death ( Pechan et al, 2002 ).…”

Hormetic response and transcriptome profiling reveal the mechanism underlying metabolic and cuticular resistance to host-specific terpenoid defences in an emerging insect pest, Pagiophloeus tsushimanus (Coleoptera: Curculionidae)

“…Plants and herbivores are continuously engaged in a struggle for survival and employ different strategies to prevent the evolution of resistance or adaptation to defensive compounds (Stahl et al, 2018). The preexisting constitutive defences in plants (e.g., toxic secondary metabolites and proteins) are everincreasingly investigated for the development of novel biopesticides (Mossa, 2016;Ntalli et al, 2019;Magalhaes et al, 2020;Maurya et al, 2020). E cient plant resistance exerts strong selection pressure on insects, which in turn develop ways to cope with the deleterious effect of phytotoxin in a stepwise process (Heckel, 2014;Heidel-Fischer and Vogel, 2015;Petschenka and Agrawal, 2016).…”