Cited by 1,358Insect Resistance and GeneticsInsect-Plant Interactions and ControlInsect Pest Control Strategies

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Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol

Mao, Ying-Bo, Cai, Wen-Juan, Wang, Jia-Wei, Hong, Gao-Jie, Tao, Xiao-Yuan, Wang, Ling-Jian, Huang, Yong-Ping, Chen, Xiao-Ya·2007·Nature Biotechnology

DOI 10.1038/nbt1352

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Abstract

We identify a cytochrome P450 gene (CYP6AE14) from cotton bollworm (Helicoverpa armigera), which permits this herbivore to tolerate otherwise inhibitory concentrations of the cotton metabolite, gossypol. CYP6AE14 is highly expressed in the midgut and its expression correlates with larval growth when gossypol is included in the diet. When larvae are fed plant material expressing double-stranded RNA (dsRNA) specific to CYP6AE14, levels of this transcript in the midgut decrease and larval growth is retarded. Both effects are more dramatic in the presence of gossypol. As a glutathione-S-transferase gene (GST1) is silenced in GST1 dsRNA-expressing plants, feeding insects plant material expressing dsRNA may be a general strategy to trigger RNA interference and could find applications in entomological research and field control of insect pests.

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Background
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Background
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Zhang, J., Li, H., Zhong, X. Y., Tian, J., Segers, A., Xia, L., & Francis, F. (2022) · Agriculture · doi:10.3390/agriculture12122108 · Cited by 23
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Noh, M. Y., Beeman, R. W., & Arakane, Y. (2011) · Entomological Research · doi:10.1111/j.1748-5967.2011.00437.x · Cited by 24
“Mao et al. (2007) targeted a cytochrome P450 gene, CYP6AE14 from cotton bollworm (Helicoverpa armigera) that is highly expressed in the midgut and has an apparent role in detoxification of gossypol, a phenol compound and cotton secondary metabolite.”
Background
Diverse Factors Affecting Efficiency of RNAi in Honey Bee Viruses
Yang, D., Xu, X. M., Zhao, H., et al. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00384 · Cited by 24
“RNAi was first discovered in transgenic plants (Mathieu and Watts, 1989), followed by the discovery of its prevalence in a wide range species (Mao et al., 2007; Miller et al., 2008; Tian et al., 2009; Garbutt et al., 2013; Ren et al., 2014).”
Background
Bxy‐fuca encoding α‐L‐fucosidase plays crucial roles in development and reproduction of the pathogenic pinewood nematode, Bursaphelenchus xylophilus
Tang, J., Ma, R., Zhu, N., Guo, K., Guo, Y., Bai, L., Yu, H., Hu, J., & Zhang, X. (2019) · Pest Management Science · doi:10.1002/ps.5497 · Cited by 25
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Progress and Opportunities of In Planta and Topical RNAi for the Biotechnological Control of Agricultural Pests
Basso, M. F., Vasquez, D. D. N., Pinto, E. R. C., Pinheiro, D. H., Cruz, B., Maktura, G. C., Guidelli, G. V., Marques‐Souza, H., & Grossi‐de‐Sá, M. F. (2025) · Agronomy · doi:10.3390/agronomy15040859 · Cited by 24
RNAi in Agriculturally-Important Arthropods
Aronstein, K. A., Oppert, B., & Lorenzen, M. D. (2011) · InTech eBooks · doi:10.5772/19768 · Cited by 23
“armigera gut and reduced larval growth (Mao et al., 2007).”
BackgroundInfluential
RNAi‐knockdown of the Locusta migratoria nuclear export factor protein results in insect mortality and alterations in gut microbiome
Xie, J., Li, S., Zhang, W., & Xia, Y. (2018) · Pest Management Science · doi:10.1002/ps.5258 · Cited by 23
Assessment on effects of transplastomic potato plants expressing Colorado potato beetle β-Actin double-stranded RNAs for three non-target pests
Ren, B., Cao, J., He, Y., et al. (2021) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2021.104909 · Cited by 23
Complete protection from Henosepilachna vigintioctopunctata by expressing long double‐stranded RNAs in potato plastids
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Double-stranded RNA degrading nuclease affects RNAi efficiency in the melon fly, Zeugodacus cucurbitae
Ahmad, S., Jamil, M., Jaworski, C. C., et al. (2023) · Journal of Pest Science · doi:10.1007/s10340-023-01637-1 · Cited by 23
“Transgenic crops that produce a dsRNA specific to the target pest species may offer alternative solutions: several crops have been protected against specific pest insects by this method (Baum et al. 2007; Mao et al. 2007; Jin et al. 2015; Zhang et al. 2015).”
Knocking down a putative Δ1 ‐pyrroline‐5‐carboxylate dehydrogenase gene by RNA interference inhibits flight and causes adult lethality in the Colorado potato beetle Leptinotarsa decemlineata (Say)
Wan, P., Fu, K., Lü, F., et al. (2014) · Pest Management Science · doi:10.1002/ps.3941 · Cited by 23
Applications of Parasitoid Virus and Venom Research in Agriculture
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“Similarly, transgenic cotton plants expressing dsRNA targeting a P450 gene expressed in the midgut of the cotton bollworm, related with the detoxification of gossypol, are resistant to Helicoverpa armigera (Mao et al., 2007).”
Background
Silencing of JHEH and EcR genes of Plutella xylostella (Lepidoptera: Plutellidae) through double stranded RNA oral delivery
Chaitanya, B. N., Asokan, R., Sita, T., et al. (2017) · Journal of Asia-Pacific Entomology · doi:10.1016/j.aspen.2017.03.020 · Cited by 23
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Development and characterization of marker‐free and transgene insertion site‐defined transgenic wheat with improved grain storability and fatty acid content
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“In addition, plantmediated RNA interference of insect genes has been successfully used to engineer the resistance to crop pests, including wheat defence to the aphid Sitobion avenae (Abdellatef et al., 2015;Mao et al., 2007; Sun et al., 2019).”
Background
The effect of silencing arginine kinase by RNAi on the larval development of Helicoverpa armigera
Qi, X.-L., Su, X., Lu, G.-Q., Liu, C. X., Liang, G.-M., & Cheng, H. M. (2015) · Bulletin of Entomological Research · doi:10.1017/s0007485315000450 · Cited by 23
“armigera, and this method could be applied in entomological research and field control of insect pests (Mao et al., 2007).”
Method
Cotton Bollworm (H. armigera) Effector PPI5 Targets FKBP17‐2 to Inhibit ER Immunity and JA/SA Responses, Enhancing Insect Feeding
Wang, Y., Zhu, C., Chen, G., Li, X., Zhu, M., Alariqi, M., Hussian, A., Ma, W., Lindsey, K., Zhang, X., et al. (2024) · Advanced Science · doi:10.1002/advs.202407826 · Cited by 23
Uniting RNAi Technology and Conservation Biocontrol to Promote Global Food Security and Agrobiodiversity
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“Transgenic and spray approaches to RNAi-based crop protection have shown promise in targeting both insect pests and pathogens (Baum et al., 2007; Mao et al., 2007; Koch et al., 2016; Head et al., 2017; Mitter et al., 2017; Worrall et al., 2019; Kuo and Falk, 2020; Petek et al., 2020).”
Background
A novel method of demonstrating the molecular and functional equivalence between in vitro and plant-produced double-stranded RNA
Urquhart, W. E. S., Mueller, G. M., Carleton, S. M., Song, Z., Perez, T., Uffman, J. P., Jensen, P. D., Levine, S. L., & Ward, J. (2015) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2015.09.004 · Cited by 23
Identification and Functional Analysis of Chitin Synthase A in Oriental Armyworm, Mythimna separata
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Evaluation of some potential target genes and methods for RNAi-mediated pest control of the corn earworm Helicoverpa zea
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Metabolic Resistance in the Fall Armyworm: An Overview
Carvalho, I. F., Erdmann, L. L., Machado, L. L., et al. (2018) · Journal of Agricultural Science · doi:10.5539/jas.v10n12p426 · Cited by 22
“Though in recent years, due to technological advances such as interference RNA technology and genome sequencing, it is being possible to investigate FAW’s CarEs specificity and functions (Mao et al., 2007; Shi et al., 2016; Gouin et al., 2017).”
Background
Negligible transcriptome and metabolome alterations in RNAi insecticidal maize against Monolepta hieroglyphica
Zhang, X., Zhang, R., Li, L., Yang, Y., Ding, Y., Guan, H., Wang, X., Zhang, A., & Wen, H. (2020) · Plant Cell Reports · doi:10.1007/s00299-020-02582-4 · Cited by 22
Non-Target Effects of dsRNA Molecules in Hemipteran Insects
Arora, A. K., Chung, S. H., & Douglas, A. E. (2021) · Genes · doi:10.3390/genes12030407 · Cited by 22
“Ground-breaking studies on corn root worm and cotton bollworm conducted over a decade ago [1,2] provided proof-of-concept for the use of RNA interference (RNAi) in insect pest control.”
Background
Insect and Nematode Resistance
Thurau, T., Ye, W., & Cai, D. (2009) · Biotechnology in agriculture and forestry · doi:10.1007/978-3-642-02391-0_10 · Cited by 22
Diet-Delivered dsRNAs for Juvenile Hormone-Binding Protein and Vacuolar ATPase-H Implied Their Potential in the Management of the Melon Aphid (Hemiptera: Aphididae)
Rebijith, K. B., Asokan, R., Ranjitha, H. H., Prasad, B. S. R., Krishna, V., & Kumar, N. K. K. (2015) · Environmental Entomology · doi:10.1093/ee/nvv178 · Cited by 24
“…proteins (Ober and Jockusch 2006), salivary gland proteins involved in digestion (Mutti et al. 2006), gut enzymes (Turner et al. 2006), hormone receptors (Cruz et al. 2006, Martin et al. 2006), or even proteins involved in host–insect interaction (Aljamali et al. 2003, Mao et al. 2007).”
Background
Genomics Era for Plants and Crop Species – Advances Made and Needed Tasks Ahead
Abdurakhmonov, I. Y. (2016) · InTech eBooks · doi:10.5772/62083 · Cited by 22
A spray-induced gene silencing strategy for Spodoptera frugiperda oviposition inhibition using nanomaterial-encapsulated dsEcR
Li, N., Xu, X., Li, J., Hull, J. J., Chen, L., & Liang, G. (2024) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2024.136503 · Cited by 22
Akt-FoxO signaling drives co-adaptation to insecticide and host plant stresses in an herbivorous insect
Zhang, H., Gao, H., Lin, X., Yang, B., Wang, J., Yuan, X., Zhang, Z., He, T., & Liu, Z. (2024) · Journal of Advanced Research · doi:10.1016/j.jare.2024.11.006 · Cited by 24
“P450 detoxiﬁcation enzymes have been demonstrated to play a role in the metabolism of various plant secondary metabolites in multiple insect species, including Helicoverpa armigera [11], Aphis gossypii [12], Nilaparvata lugens [13].”
RNA interference (RNAi) for insect pest management: understanding mechanisms, strategies, challenges and future prospects
Mahanta, D. K., Komal, J., Bhoi, T. K., Samal, I., Dash, S., & Jangra, S. (2025) · Biologia Futura · doi:10.1007/s42977-025-00281-3 · Cited by 21
“Furthermore, HIGS targeting the CYP6AE14 gene, a cytochrome P450 gene, was successful in controlling the cotton bollworm ( Helicoverpa armigera ) in both transgenic Arabidopsis and tobacco plants (Mao et al. 2007).”
Generation of a Transcriptome in a Model Lepidopteran Pest, Heliothis virescens, Using Multiple Sequencing Strategies for Profiling Midgut Gene Expression
Perera, O. P., Shelby, K. S., Popham, H. J. R., Gould, F. L., Adang, M. J., & Jurat‐Fuentes, J. L. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128563 · Cited by 20
RNA Interference to Control Asian Corn Borer Using dsRNA from a Novel Glutathione-S-Transferase Gene of Ostrinia furnacalis (Lepidoptera: Crambidae)
Zhang, Y., Zhang, Y., Fu, M., et al. (2018) · Journal of Insect Science · doi:10.1093/jisesa/iey100 · Cited by 21
A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite
Huber, M., Roder, T., Irmisch, S., Riedel, A., Gablenz, S., Fricke, J., Rahfeld, P., Reichelt, M., Paetz, C., Liechti, N., et al. (2021) · eLife · doi:10.7554/elife.68642 · Cited by 21
Silencing of vitellogenin gene contributes to the promise of controlling red palm weevil, Rhynchophorus ferrugineus (Olivier)
Rasool, K. G., Mehmood, K., Tufail, M., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-01159-9 · Cited by 21
Strong Fitness Costs of Fall Armyworm Resistance to Dual-Gene Bt Maize Are Magnified on Less-Suitable Host-Crop Cultivars
Santos‐Amaya, O. F., Tavares, C. S., Rodrigues, J. V. C., de Oliveira, E. E., Guedes, R. N. C., & Pereira, E. J. G. (2022) · Agronomy · doi:10.3390/agronomy12030682 · Cited by 23
Plastid Transformation of Micro-Tom Tomato with a Hemipteran Double-Stranded RNA Results in RNA Interference in Multiple Insect Species
Kaplanoglu, E., Kolotilin, I., Menassa, R., & Donly, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23073918 · Cited by 21
“However, this approach can be limited in its effectiveness, as dsRNA transcribed in the nucleus first enters the plant’s own RNAi pathway and is processed into siRNA molecules in the cytosol [6,16].”
Background
A comprehensive review on Gossypium hirsutum resistance against cotton leaf curl virus
Nadeem, S., Ahmed, S. R., Luqman, T., et al. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1306469 · Cited by 21

Authors: Mao, Y.-B., Cai, W.-J., Wang, J.-W., Hong, G.-J., Tao, X.-Y., Wang, L.-J., Huang, Y.-P., & Chen, X.-Y.
Affiliations: Chinese Academy of Sciences (CN)
Corresponding author: Chen, Xiao-Ya
ORCID: Mao, Ying-Bo
Wang, Ling-Jian
Chen, Xiao-Ya
Venue: Nature Biotechnology
Publisher: Springer Science and Business Media LLC
Published: 2007-11
Volume: 25
Issue: 11
Pages: 1307-1313
ISSN: 0733-222X (ISSN-L)
1087-0156
1546-1696
DOI: 10.1038/nbt1352
OpenAlex: W2121440246
Cited by: 1,358
References: 50
Citations by year: 2026: 44 · 2025: 76 · 2024: 80 · 2023: 56 · 2022: 111 · 2021: 98 · 2020: 84 · 2019: 87 · 2018: 67 · 2017: 95 · 2016: 92 · 2015: 89 · 2014: 84 · 2013: 77 · 2012: 68
FWCI: 13.10
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Biotechnology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Insect Resistance and Genetics
Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect-Plant Interactions and Control
Life Sciences › Agricultural and Biological Sciences › Plant Science › Insect Pest Control Strategies
Keywords: Helicoverpa armigera, cytochrome P450 monooxygenase, dsRNA feeding, midgut gene expression, larval growth, insect pest control, plant-insect interactions
MeSH terms: Animals, Gossypium, Cytochrome P-450 Enzyme System, Digestion, Drug Resistance, Glutathione Transferase, Gossypol, Larva, Lepidoptera, Molecular Sequence Data, Pest Control, Biological, RNA, Double-Stranded, Nicotiana, Arabidopsis, RNA, Plant, Insect Proteins, Gene Silencing, Plants, Genetically Modified, RNA Interference, RNA, Small Interfering, Cytochrome P-450 Enzyme Inhibitors

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Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol

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