Helicoverpa armigera herbivory negatively impacts Aphis gossypii populations via inducible metabolic changes

Abstract

BACKGROUND: Helicoverpa armigera and Aphis gossypii are two important insect species that feed on cotton plants. These insects have distinct abilities to induce plant resistance and tolerate plant toxins, which results in interspecific competition imbalance that may be fatal to the low-tolerance A. gossypii and force these insects to develop avoidance behaviors and subsequently separate from their niche. We implemented ecological experiments to test the effects of H. armigera-induced plant resistance and behavioral avoidance in A. gossypii, and employed transcriptomics and metabolomics analyses to reveal changes in resistance genes and metabolites in plants.RESULTS: Our results demonstrate that cotton plants induced by H. armigera cause significant inhibitory and avoidance effects on A. gossypii insect populations. Electrical penetration graph (EPG) analysis showed changes in plant resistance induced by H. armigera leading to a decreased feeding efficiency of A. gossypii. In addition, genes associated with jasmonic acid and ethylene signaling pathways were significantly up-regulated in cotton plants after H. armigera induction, which led to a significant up-regulation of metabolites inducing plant resistance. These observations were corroborated by bioactivity analysis on metabolites, which showed that jasmonic acid, gossypol and tannins have significant inhibitory effects on A. gossypii populations. In contrast, methylparaben is associated with avoidance behaviors on A. gossypii populations.CONCLUSION: Our study suggests that the differences in the ability to induce plant resistance and tolerance between two non-predatory insects were lethal to low-tolerance A. gossypii insects, which might be a major factor determining their niche differentiation. This was further demonstrated by screening anti-insect and bio-hormonal metabolites. Our study provides a reference for investigating the evolutionary relationship between non-predatory insects and insights to implement effective insect biocontrol.

Defense Responses of Different Rice Varieties Affect Growth Performance and Food Utilization of Cnaphalocrocis medinalis Larvae

“…ROS accumulation can induce plants to exhibit stimulated antioxidant enzyme activity activities such as phenylalanine ammonia lyase (PAL) and glutathione reductase, leading to an increase in the production of secondary metabolites such as flavonoids and tannins (Gautam et al 2023 ; Ho et al 2020 ; Han and Yuan 2004 ). These secondary metabolites have negative impacts on insect populations, such as inhibiting insect development, increasing mortality, reducing feeding efficiency, and decreasing protein utilization efficiency (Gautam et al 2023 ; Mierziak et al 2014 ; Zheng et al 2022 ). Cheah et al ( 2020 ) found that the accumulation of PAL potentially enhances the resistance of a C. medinalis -resistant rice variety (Qingliu) by priming the biosynthesis of essential flavonoids.…”

Integrated Omics Analysis Reveals Key Pathways in Cotton Defense against Mirid Bug (Adelphocoris suturalis Jakovlev) Feeding

“…Potted cotton plants (G. hirsutum CCRI 49) were transplanted into soil pots (15 × 17 cm), then put it into environmentally controlled chambers (50 × 60 × 110 cm) and maintained under either a 14 h (long day) or 10 h (short day) light period at 25 ± 2 • C and 65-70% relative humidity till the plants reached the four-leaf stage for further testing [13]. Subsequently, each cotton plant was placed in a 30 cm squared cage, and nine adult A. suturalis (starved for 12 h before inoculation) were introduced onto the leaves.…”

“…Increasing evidence suggests that the JA signaling pathway is crucial in plant defense, contributing to rice resistance against the leaf folder (Cnaphalocrocis medinalis) [12]. JA also mediates cotton plant resistance induced by Helicoverpa armigera and affects the growth and development of Aphis gossypii [13]. When rice plants are attacked by the brown plant hopper (Nilaparvata lugens), JA activates rice defense responses and gibberellin catabolism [14].…”

Gut yeast diversity of Helicoverpa armigera (Lepidoptera: Noctuidae) under different dietary conditions

“…Helicoverpa armigera (Lepidoptera: Noctuidae) is a worldwide pest known to infest over 200 host plants, including cotton, tomato, pepper, potato, and various other crops and wild plants ( Zheng et al, 2022 ). It occurs frequently in large crop-growing countries such as China, India, and Australia.…”