Insight into the bioactivity and action mode of betulin, a candidate aphicide from plant metabolite, against aphids

The peach aphid is one of the most harmful pests worldwide and can parasitize over 400 species of plants. In addition to sucking phloem sap and secreting honeydew, the peach aphid can also spread various plant viruses, causing severe crop yield reductions and huge economic losses.

So far, the control of peach aphids mainly relies on chemical pesticides. However, the long-term and unreasonable use of these chemicals has led to environmental pollution and prompted aphids to develop resistance to pesticides, making the control of these insects even more difficult. Therefore, it is imperative to develop new, environmentally friendly insecticides.

For example, secondary plant metabolites, such as betulin – which is a key bioactive compound in aphid-resistant wild peach – have been proven to be highly toxic to aphids, demonstrating significant potential for development as a green insecticide. To find out how exactly betulin acts against aphids, Wang et al. used a combination of field trials and molecular, genetic and electrophysiological approaches.

The results showed that betulin inhibits the expression of MpGABR – a gene that helps regulate nerve signals in aphids – while simultaneously suppressing the function of the MpGABR protein by binding to its specific structural component called THR228. Exposing aphids to betulin significantly inhibited the expression of MpGABR. Micro-scale thermophoresis (a technique used to measure the binding between molecules) and voltage clamp experiments (used to study how compounds affect ion channel activity) confirmed that betulin could bind to the MpGABR protein via THR228 and acted as its inhibitor. Molecular docking (a computer method that predicts how a molecule interacts with a protein), mutagenesis analysis, and genome editing studies further suggested that THR228 is a key site that has remained nearly unchanged in aphid through evolution because it is essential for the protein’s function.

The findings of Wang et al. will be beneficial for pesticide companies for developing new products, helping farmers control aphids and avoiding environmental pollution. More research is needed before these benefits can be realized, such as solvent formulation trials for developing betulin as an aphid insecticide, regional trials for using betulin as an aphid insecticide, and screening for insecticides with similar functions to this metabolite.

Over more than 400 million years of coevolution with herbivores, plants have developed a variety of morphological (Soujanya et al., 2023), biochemical (Zhou et al., 2024b), and molecular (Wang et al., 2024) defense strategies against insect herbivore attack. Plant secondary metabolites are highly valuable natural compounds, offering abundant and potent biochemical defense driven by plant-insect coevolution (Jahan et al., 2025). Interestingly, wild relatives of crops with insect resistance usually accumulate large amounts of biologically active compounds (Alonso-Salces et al., 2022; Wang et al., 2022a). Accordingly, investigating the bioactivities and potential mechanisms of action of compounds derived from wild resistant germplasms may provide effective and sustainable strategies for pest control in crop protection.

Myzus persicae (Sülzer) is one of the most destructive sap-feeding pests worldwide. It is able to settle on more than 400 plant species globally, displaying extraordinary polyphagia and a wide range of hazards (Bass et al., 2014). In addition to ingesting phloem saps and secreting honeydew, M. persicae can transmit various plant viruses (Guo et al., 2022), resulting in severe losses in crop yields. To date, the principal control strategy for M. persicae has relied on synthetic insecticides, including pyrethroids, organophosphorus compounds, carbamates, and neonicotinoids (Jiménez-Jiménez et al., 2019; Martins et al., 2021; Zhang et al., 2023). However, long-term irrational application of these chemical insecticides has led to environmental pollution and promoted the resistance of aphids to insecticides (Troczka et al., 2021; Zhang et al., 2023; Stará et al., 2024). Therefore, it is necessary to develop novel green insecticides as potential alternatives to synthetic insecticides. Fortunately, plant secondary metabolites are a ‘treasure trove of active compounds’ that serve as a rich resource for the development of promising green insecticides.

Our previous study revealed that Prunus davidiana, a close wild relative of cultivated peach, displays strong resistance to M. persicae through the accumulation of high levels of betulin (Wang et al., 2022a; Wang et al., 2024). In addition, betulin, a lupane-type triterpene, possesses strong insecticidal activity and is a promising substance for the development of novel aphid-control insecticides. A number of studies have reported that betulin and its derivatives exhibit a wide range of pharmacological activities (Amiri et al., 2020). An immune stimulant, Ir-Bet, was prepared using iridium complex and betulin, which evoked ferritinophagy-enhanced ferroptosis, thereby activating anti-tumor immunity (Lv et al., 2023). The anti-inflammatory effect of betulin has been reported in macrophages at lymphoma sites in mice (Szlasa et al., 2023). Betulin has been found to improve hyperlipidemia and insulin resistance and decrease atherosclerotic plaques by inhibiting the maturation of sterol regulatory element-binding protein (Tang et al., 2011). Additionally, betulin and its derivatives have been found to exhibit insecticidal activity against Plutella xylostella L. (Huang et al., 2025), Aedes aegypti (de Almeida Teles et al., 2024), and Drosophila melanogaster (Lee and Min, 2024). However, the insecticidal mechanism of betulin against aphids remains unclear.

Gamma-aminobutyric acid (GABA) receptors have been confirmed to be targets of terpenoids that impair neuronal function in insect herbivores (Guo et al., 2023). There are two types of GABA receptors: ionotropic (GABA_A) and metabotropic (GABA_B) receptors. The first GABA receptor subunit identified in insects is encoded by Rdl, which confers resistance to dieldrin in D. melanogaster (Ffrench-Constant et al., 1991). Although a variety of terpenoids play roles as positive allosteric modulators or noncompetitive antagonists (NCAs) of GABA_A receptors (GABRs) (Guo et al., 2023), whether betulin targets the GABR in M. persicae needs to be further investigated. GABRs are heteropentameric ligand-gated ion channels in the central nervous system that conduct chloride and bicarbonate ions and are the target of numerous drugs for the treatment of neuropsychiatric disorders (Thompson, 2024). GABRs are composed of five different types of subunits, each with four helical transmembrane domains (TM1-TM4), of which TM2 is located at the center of the pentamer and forms an ion channel (Fan et al., 2024). A previous study has proposed that vertebrate and human GABR genes maintain a broad and conservative gene clustering pattern, while in invertebrates, this pattern is missing, indicating that these gene clusters were formed early in vertebrate evolution and were established after invertebrates diverged. Notably, invertebrates each possess a unique GABR gene pair, which is homologous with human GABR α and β subunits, suggesting that the existing GABR gene cluster evolved from an ancestral α-β subunit gene pair (Tsang et al., 2007). During the coevolution of plants and insects, the duplications and amino acid substitutions in GABR may have been beneficial for adaptation to insecticides and terpenoid compounds (Guo et al., 2023).

In this study, betulin was confirmed to have excellent control efficacy against M. persicae in both greenhouse and field experiments. RNA-seq, quantitative real-time PCR (qRT-PCR), and western blotting assays revealed that betulin significantly inhibited the expression of MpGABR in aphids. In addition, RNAi-mediated silencing of MpGABR markedly increased aphid sensitivity to betulin. Furthermore, microscale thermophoresis (MST) and voltage-clamp assays indicated that betulin can bind to MpGABR (K_d = 2.24 µM) and act as an inhibitor (EC₅₀=20.66 µM) of MpGABR. Molecular docking analysis suggested that betulin bound to MpGABR via the THR228 amino acid residue. This site is highly conserved across 11 species in the Aphididae family of Hemiptera and may be a critical specific binding site for betulin in MpGABR in aphids. Mutagenesis and genome editing experiments revealed that betulin bound specifically to this amino acid residue in aphids but not in Drosophila, resulting in aphid death. This study elucidated the insecticidal mechanism of betulin involving the targeting of MpGABR, providing a sustainable green strategy for aphid control. However, given that betulin may affect a wider range of organisms, it should be used with caution.

Although chemical pesticides are effective in pest control, the long-term unreasonable application of these substances has led to the emergence of resistant pests, environmental deterioration, and deleterious effects on nontarget organisms, including humans, raising widespread and intense concerns (Devi et al., 2022). These challenges have made it urgent for the development of alternative strategies for pest control. Recently, the utilization of plant secondary metabolites as insecticides has become increasingly popular as an eco-friendly and biocontrol approach (Ling et al., 2022; Ayilara et al., 2023). Our previous study revealed that P. davidiana, a wild relative of cultivated peach, strongly resists M. persicae by accumulating high contents of betulin (Wang et al., 2022a; Wang et al., 2024). In addition, betulin, a lupane-type triterpene, possesses potent insecticidal activity and is a promising substance for the development of novel insecticides for aphid control. In this study, the insecticidal effect of betulin was further evaluated by comparing the control efficacy of betulin with that of pymetrozine against aphids in greenhouses and fields (Figure 1A–G). These results indicate that betulin has a similar control effect to pymetrozine and has immense potential for development as a plant-derived insecticide.

Terpenes are a diverse group of plant secondary metabolites that can increase the resistance of plants to insect herbivores through direct (Wang et al., 2025a) and indirect (Wang et al., 2025b) defense mechanisms. In direct defense against herbivores, triterpenes play important roles in diverse biological activities, including antiparasitic, insecticidal, and antifeedant activities (Tian et al., 2021; Kuzminac et al., 2023). Azadirachtin, a tetracyclic triterpenoid compound isolated from the Indian neem tree (Azadirachta indica), is one of the most prominent commercial biopesticides, exhibiting strong insect antifeedant properties, as well as growth- and reproduction-regulating effects (Dawkar et al., 2019; Bae et al., 2022). Besides, triterpene glycoside compounds play crucial roles in the defense of tobacco (Nicotiana attenuata) against tobacco hornworm (Manduca sexta) larvae (Yang et al., 2024). Although betulin exhibits various pharmacological activities (Amiri et al., 2020; Li et al., 2022; Yan et al., 2022; Lv et al., 2023), reports on its insecticidal activity are limited. Encouragingly, the effects of betulin and its derivatives on pests have attracted increasing attention. Betulinic acid and its derivatives showed larvicidal activity against A. aegypti larvae (da Silva et al., 2016). Betulin-cinnamic acid-related hybrid compound 5b exhibited strong aphicidal activity, and compound 2l could destroy the ultrastructure of midgut cells and significantly inhibit the activity of α-amylase in diamondback moth (Pl. xylostella L.) larvae (Huang et al.). Our previous studies also indicated that betulin possesses potent insecticidal activity and is a key endogenous secondary metabolite related to the defense of peach against M. persicae (Wang et al., 2022a). Elucidating the insecticidal mechanism of betulin against aphids will provide a basis for the development of novel aphicides and sustainable strategies for aphid control.

GABA receptors have been confirmed to be targets of terpenoids that impair insect neuronal function in herbivores (Guo et al., 2023). GABRs are heteropentameric ligand-gated ion channels in the central nervous system that conduct chloride and bicarbonate ions. These receptors are targets of numerous drugs for the treatment of neuropsychiatric disorders (Thompson, 2024). A variety of terpenoids act as positive allosteric modulators or NCAs of GABRs, such as diterpenoids (isopimaric acid and miltirone), sesquiterpenoids (picrotoxin, bilobalide, and ginkgolides), and monoterpenoids (α-thujone and thymol) (Guo et al., 2023). In this study, both GO and KEGG enrichment analyses revealed that the DEGs identified by RNA-seq were enriched in GABAergic signaling-related pathways (Figure 2F and G). Additionally, the expression of the DEGs related to GABRs, particularly MpGABR (Figure 2—source data 1), in the betulin group was significantly lower than that in the CK group (Figure 2H). Besides, the relative expression of MpGABR, MpGABRAP, and MpGABRB decreased gradually after M. persicae was exposed to the LC₃₀, LC₅₀, and LC₇₀ of betulin for 48 hr (Figure 3B–D). Among them, MpGABR was the most sensitive to betulin, and its expression was reduced by 82.91% after exposure to the LC₃₀ of betulin for 48 hr. Furthermore, compared with the control group, the M. persicae group with MpGABR silenced by RNAi presented a significant increase in mortality (p<0.001), by 30.44%, after 48 hr of exposure to the LC₅₀ of betulin (Figure 4E). Collectively, these results suggest that betulin may have insecticidal effects on aphids by inhibiting MpGABR expression. The regulation of gene expression is sophisticated and delicate (Pope and Medzhitov, 2018). The regulatory network controlling GABR expression remains unclear. In adult rats, epileptic seizures have been reported to increase the levels of brain-derived neurotrophic factor, which in turn prompted the transcription factors CREB and ICER to reduce the gene expression of the GABR α1 subunit (Lund et al., 2008). In Drosophila, it has been demonstrated that WIDE AWAKE, which regulated the onset of sleep, interacted with the GABR and upregulated its expression level (Liu et al., 2014). In the Drosophila brain, circular RNA circ_sxc was found to inhibit the expression of miR-87-3-p in the brain through sponge adsorption, thereby regulating the expression of neurotransmitter receptor ligand proteins, including GABR, and ensuring the normal function of synaptic signal transmission in brain neurons (Li et al., 2024). However, it remains unclear how betulin reduces MpGABR expression, and further research is needed.

Additionally, betulin has been reported to be able to bind to GABRs (Manayi et al., 2016). We further investigated the interaction of betulin with the MpGABR protein. The MST assay revealed that betulin was able to bind to MpGABR (K_d = 2.24 µM) (Figure 6B), which is consistent with previous findings showing that betulin binds to GABA receptors in mouse brains in vitro (Muceniece et al., 2008). Voltage-clamp-based electrophysiological recordings indicated that betulin acted as an inhibitor (EC₅₀=20.66 µM) for MpGABR (Figure 6C and D). Subsequent molecular docking analysis suggested that four key amino acid residues (ARG224, ALA226, PHE227, and THR228) interact with betulin in the MpGABR binding pocket (Figure 7A), among which merely ALA226 and THR228 interact with betulin via hydrogen bonding (Figure 7—source data 1). The results of the sequence alignment revealed that only THR228 was conserved across 11 species in the Aphididae family of Hemiptera (Figure 7B). Furthermore, evaluation of the ability of betulin to bind to MpGABR mutants with mutations at those four sites revealed that the ability of betulin to bind to T228R was significantly weaker than its ability to bind to the WT (Figure 7D and E, Figure 7—source data 2), indicating that THR228 is an essential specific site for the binding of betulin to MpGABR. Moreover, to further prove that THR228 is the specific binding site for betulin in MpGABR, the binding affinities of betulin with the WT and mutant (R122T, equivalent to THR228 in MpGABR) Drosophila DmGABR proteins were assessed using MST. The results showed that betulin was able to bind to DmGABR^R122T (K_d = 342.4 µM) but not DmGABR^WT (Figure 8B). Additionally, after exposure to different concentrations of betulin, the mortality rate of DmGABR^R122T Drosophila was significantly greater than that of DmGABR^WT Drosophila (Figure 8E, Figure 8—source data 1). Similarly, a previous study indicated that the R122G amino acid site substitution, generated via RNA editing, affects the sensitivity of Drosophila to fipronil (Es-Salah et al., 2008). Together, these findings suggest that betulin binds specifically to MpGABR via THR228, acting as an inhibitor of MpGABR and causing aphid death. Studies on key amino acids that are crucial for GABR function have primarily focused on transmembrane regions. For instance, based on the mutational research and Drosophila GABR modeling approach, multiple key amino acids have been identified as insecticide targets in the transmembrane domain (Nakao and Banba, 2021). Guo et al., 2023 proposed that amino acid substitutions in transmembrane domain 2 contribute to terpenoid insensitivity during plant-insect coevolution. However, these studies have neglected the extracellular domain. Our study signified that betulin targets the THR228 site in the extracellular domain of MpGABR, which is conserved only in the Aphididae family. Therefore, betulin is speculated to be a specific insecticidal substance evolved by plants in response to aphid infestation. Besides, further verification is needed to determine whether betulin is toxic to other insect species.

GABRs belong to the cysteine loop (Cys)-loop superfamily of neurotransmitter receptors and are essential heteropentameric ligand-gated ion channels in the central nervous system. After GABA binds to the extracellular Cys-loop of a GABR (Ashby et al., 2012), the GABR is activated and opens up its central pore to allow chloride ions to pass through, thereby hyperpolarizing neurons and attenuating excitatory neurotransmission (Tremblay et al., 2016). In insects, GABRs play important roles in circadian rhythms (Schellinger et al., 2022), sleep (Chaturvedi et al., 2022), movement (Eick et al., 2022), and olfactory memory (Yamagata et al., 2021). Additionally, GABR is a critical target for a variety of insecticides and ectoparasiticides. Insecticides targeting GABRs are categorized into NCAs and competitive antagonists (CAs) according to their different binding sites. NCAs block chloride channels in nerve cells by interacting with amino acid residues of the GABA-gated chloride channel, causing a conformational change in the receptor, which interferes with the normal function of the central nervous system and ultimately leads to insect death (Nakao and Banba, 2021; Guo et al., 2023). A series of first- and second-generation NCA insecticides have been successfully developed. Picrotoxinin, isolated from Anamirta cocculus fruit, is the oldest natural NCA and is toxic to houseflies (Tong et al., 2023). Among the first-generation NCAs, polychlorocycloalkanes, including dieldrin and lindane, were commonly used as pesticides in the middle and late 20th centuries (Hainzl et al., 1998; Tanaka, 2019). As second-generation NCAs, fipronil and its derivatives are commercially available phenylpyrazole insecticides that have been widely used for agricultural pest control (Sheng et al., 2018; Li et al., 2021). Additionally, CAs bind to orthogonal binding sites, such as the GABA recognition site in the extracellular region, competitively inhibiting the binding of GABA to its receptor, leading to toxic effects in insects. Given the lack of interference from existing insect resistance mechanisms, CAs hold promise for the development of efficient new insecticides. Novel 1,6-dihydro-6-iminopyridazine-derived insecticides, as CAs, have insecticidal properties against common cutworms and houseflies (Liu et al., 2022). Besides, nootkatone, a sesquiterpenoid, also acts as a CA to induce insect mortality (Norris et al., 2022). Fluralaner, an isooxazoline ectoparasiticide, inhibits both parasites and A. aegypti by acting as a CA (Wang et al., 2022b; Asahi et al., 2023). Our results revealed that the binding site (THR228) for betulin in MpGABR was located in the extracellular neurotransmitter-gated ion-channel ligand-binding domain (Figure 7—figure supplement 1), implying that betulin acts as a CA of MpGABR. Although the mechanism by which betulin competes with GABA for binding to MpGABR requires further experimental validation, our work may have provided a novel target for developing insecticides. In this study, betulin, on the one hand, inhibited the expression of MpGABR and, on the other hand, specifically bound to MpGABR through THR228, acting as an inhibitor of MpGABR and causing aphid death (Figure 9).

Figure 9

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The development of bioinsecticides should not only focus on the toxic effects of active substance on target organisms, but also on their influence on the ecosystem (Haddi et al., 2020). Although our results indicate that betulin has specific toxicity to aphids, previous studies have reported that betulin and its derivatives had effects on P. xylostella L. (Huang et al., 2025), A. aegypti (de Almeida Teles et al., 2024), and D. melanogaster (Lee and Min, 2024). Therefore, further research is needed to determine whether there are other insecticidal mechanisms or off-target effects of betulin. Additionally, betulin exhibits a wide range of pharmacological activities (Amiri et al., 2020), which have been used to treat various diseases, such as cancer (Lv et al., 2023), glioblastoma (Li et al., 2022), inflammation (Szlasa et al., 2023), and hyperlipidemia (Tang et al., 2011). Before applying betulin in the field, it is necessary to fully verify and consider whether betulin has any impact on farmers’ health. Furthermore, will betulin cause residue or diffusion during the field application process? Will long-term application promote the evolution of resistance to aphids or other insects? These issues also need further experimental verification. In summary, before any field application, further research on the environmental behavior, degradation process, and safety of betulin is needed.

RNA sequence data were deposited in NCBI (accession number PRJNA1334570). All data generated or analyzed during this study are included in the manuscript and supporting files.

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Author details

1. Junxiu Wang

   Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Chongqing Key Laboratory of Forest Ecological Restoration and Utilization in the Three Gorges Reservoir Area, College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

   Contribution

   Data curation, Funding acquisition, Visualization, Writing – original draft, Writing – review and editing

   Contributed equally with

   Matthana Klakong

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6453-3477

2. Matthana Klakong

   College of Plant Protection, Southwest University, Chongqing, China

   Contribution

   Data curation, Validation, Investigation, Methodology

   Contributed equally with

   Junxiu Wang

   Competing interests

   No competing interests declared

3. Qiuyu Zhu

   College of Plant Protection, Southwest University, Chongqing, China

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

4. Jinting Pan

   Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Chongqing Key Laboratory of Forest Ecological Restoration and Utilization in the Three Gorges Reservoir Area, College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

   Contribution

   Methodology

   Competing interests

   No competing interests declared

5. Yudie Duan

   Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Chongqing Key Laboratory of Forest Ecological Restoration and Utilization in the Three Gorges Reservoir Area, College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

   Contribution

   Methodology

   Competing interests

   No competing interests declared

6. Lirong Wang

   Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, China

   Contribution

   Resources

   Competing interests

   No competing interests declared

7. Yong Li

   Zhengzhou Fruit Research Institute, Chinese Academy of Agricultural Sciences, Zhengzhou, China

   Contribution

   Resources

   Competing interests

   No competing interests declared

8. Jiangbo Dang

   Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Chongqing Key Laboratory of Forest Ecological Restoration and Utilization in the Three Gorges Reservoir Area, College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

9. Danlong Jing

   Key Laboratory of Agricultural Biosafety and Green Production of Upper Yangtze River (Ministry of Education), Chongqing Key Laboratory of Forest Ecological Restoration and Utilization in the Three Gorges Reservoir Area, College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China

   Contribution

   Writing – review and editing

   Competing interests

   No competing interests declared

10. Hong Zhou

    1. College of Plant Protection, Southwest University, Chongqing, China
    2. Yibin Academy of Southwest University, Yibin, China

    Contribution

    Data curation, Supervision, Funding acquisition, Visualization, Writing – original draft, Writing – review and editing

    For correspondence

    zhouhong1990@swu.edu.cn

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0003-2438-622X

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