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
Collaborative contribution of six cytochrome P450 monooxygenase genes to fenpropathrin resistance in Tetranychus cinnabarinus (Boisduval)
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Background
Small Luggage for a Long Journey: Transfer of Vesicle-Enclosed Small RNA in Interspecies Communication
Lefebvre, F. A., & Lécuyer, É. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00377 · Cited by 53
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BackgroundInfluential
Transcription factor aryl hydrocarbon receptor / aryl hydrocarbon receptor nuclear translocator is involved in regulation of the xenobiotic tolerance‐related cytochrome P450 CYP6DA2 in Aphis gossypii Glover
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Background
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Runo, S. M., Alakonya, A. E., Machuka, J. S., & Sinha, N. R. (2010) · Pest Management Science · doi:10.1002/ps.2052 · Cited by 49
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“…made to target various genes in several insect species such as Diabrotica virgifera virgifera (Baum et al., 2007), Myzus persicae (Pitino et al., 2011; Mao & Zeng, 2014; Coleman et al., 2015), Sitobion avenae (Xu et al., 2014) and H. armigera (Mao et al., 2007; Mao et al., 2011; Liu et al., 2015).”
Background
Insect-Resistant Transgenic Crops and Biological Control
Romeis, J., Driesche, R. G. V., Barratt, B. I. P., & Bigler, F. (2008) · Springer eBooks · doi:10.1007/978-1-4020-8373-0_4 · Cited by 50
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“…through artificial feeding of siRNAs/dsRNAs, and through transient or stable transformation of plants expressing interfering RNAs (Bucher et al., 2002; Araujo et al., 2006; Mutti et al., 2006; Jaubert-Mao et al., 2007; Possamai et al., 2007; Mao et al., 2011; Pitino et al., 2011; Zha et al., 2011).”
Background
Host-induced silencing of the Colletotrichum gloeosporioides conidial morphology 1 gene (CgCOM1) confers resistance against Anthracnose disease in chilli and tomato
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“During the last decade, many studies have proven that RNAi technology is efficient in pest control mainly via transgenic plants, feeding, trunk injection, or spraying [56,57,174,175].”
Background
Characterization of two NADPH: Cytochrome P450 reductases from cotton (Gossypium hirsutum)
Yang, C., Lu, S., Mao, Y., et al. (2009) · Phytochemistry · doi:10.1016/j.phytochem.2009.09.026 · Cited by 48
“These secondary metabolites function as phytoalexins and protect the plants against pathogens and herbivores (Essenberg et al., 1990; Mao et al., 2007).”
Background
Characterization and RNAi-mediated knockdown of Chitin Synthase A in the potato tuber moth, Phthorimaea operculella
Mohammed, A., Diab, M. R., Abdelsattar, M., & Khalil, S. M. S. (2017) · Scientific Reports · doi:10.1038/s41598-017-09858-y · Cited by 49
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“Larvae were fed on artificial diet, as previously described by Mao et al. (2007) [42].”
BackgroundMethodResult
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Background
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Asokan, R., Chandra, G. S., Manamohan, M., et al. (2013) · Journal of Pest Science · doi:10.1007/s10340-013-0541-7 · Cited by 47
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“RNAi occurs widely in eukaryotic organisms and previous studies have demonstrated that feeding-based RNAi can specifically induce an RNAi response in several insect species, such as S. exigua (Chen et al., 2008), H. armigera (Mao et al., 2007) andDiabrotica virgifera virgifera (Alves et al., 2010).”
Background
Transcriptome profiling reveals differential gene expression of detoxification enzymes in a hemimetabolous tobacco pest after feeding on jasmonate-silenced Nicotiana attenuata plants
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Background
RNA interference of carboxyesterases causes nymph mortality in the Asian citrus psyllid, Diaphorina citri
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Background
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Background
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Background
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Background
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Background
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“…their previous studies using plant-mediated RNAi to silence H. armigera CYP6AE14 transcripts, impair tolerance to gossypol and reduce larval growth (Mao et al. 2007, 2010), Tao et al. (2012) have now demonstrated that silencing of gossypoland deltamethrin-inducible CYP9A14 transcripts impairs…”
Background
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“(E) Effect of CYP6 30 pM dsRNA on YSB larval mortality at different time intervals, * Indicates that larval mortality in treatments were significantly different (N = 4, F = 9.13, DF = 18, P 0.007) from control larval mortality.”
BackgroundResultInfluential
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Background
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Background
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Background
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“Mao et al. (2007) , for example, transformed cotton to express double-stranded RNA specific to a cytochrome P450 gene from Helicoverpa armigera (Hubner) involved in detoxifying gossypol.”
Background
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Background
FoxO Transcription Factor Regulate Hormone Mediated Signaling on Nymphal Diapause
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“Targeting a gene using RNAi may reveal its function, and this method has been most recently used for agricultural pest control (Baum et al., 2007; Mao et al., 2007).”
Method
Spray-induced gene silencing: an innovative strategy for plant trait improvement and disease control
Vetukuri, R. R., Dubey, M. K., Kalyandurg, P. B., et al. (2021) · Crop Breeding and Applied Biotechnology · doi:10.1590/1984-70332021v21sa24 · Cited by 44
“SIGS against insect pests The application of RNAi for controlling insect pests has been proposed for over a decade (Baum et al. 2007, Mao et al. 2007).”
Background
Fate and transport of biological microcontaminants bound to microplastics in the soil environment
Maguire, L. W., & Gardner, C. M. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.164439 · Cited by 45
Exogenous dsRNA-Mediated RNAi: Mechanisms, Applications, Delivery Methods and Challenges in the Induction of Viral Disease Resistance in Plants
Venu, E., Ramya, A., Babu, P. L., Srinivas, B., Kumar, S., Reddy, N. K., Babu, Y. M., Majumdar, A., & Manik, S. (2024) · Viruses · doi:10.3390/v17010049 · Cited by 50
“Non-transformative methods like spray-induced gene silencing (SIGS) provide eco-friendly, transgenic-free alternatives [91,133].”
RNA interference of the P450 CYP6CM1 gene has different efficacy in B and Q biotypes of Bemisia tabaci
Li, J., Li, X., Bai, R., et al. (2014) · Pest Management Science · doi:10.1002/ps.3903 · Cited by 44
Artificial miRNA-mediated silencing of ecdysone receptor (EcR) affects larval development and oogenesis in Helicoverpa armigera
Yogindran, S., & Rajam, M. V. (2016) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2016.07.009 · Cited by 46
“Mao et al. (2007) reported larval mortality and considerable reduction in transcript levels of P450 monoxygenase gene when plant-expressed dsRNAs were fed to H. armigera larvae.”
Background
Interaction of Ferulic Acid with Glutathione S-Transferase and Carboxylesterase Genes in the Brown Planthopper, Nilaparvata lugens
Yang, J., Sun, X., Yan, S.-Y., Pan, W.-J., Zhang, M., & Cai, Q. (2017) · Journal of Chemical Ecology · doi:10.1007/s10886-017-0859-3 · Cited by 44
“armigera specific to gossypol (Mao et al. 2007), and for NlGST1–1 in BPH specific to gramine (Sun”
Background
RNAi-Mediated Knockdown of Chitin Synthase 1 (CHS1) Gene Causes Mortality and Decreased Longevity and Fecundity in Aphis gossypii
Ullah, F., Gul, H., Wang, X., et al. (2019) · Insects · doi:10.3390/insects11010022 · Cited by 44
Functional characterization of chitin deacetylase 1 gene disrupting larval–pupal transition in the drugstore beetle using RNA interference
Yang, W., Xu, K.-K., Yan, X., et al. (2018) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/j.cbpb.2018.03.001 · Cited by 43
A sequence complementarity-based approach for evaluating off-target transcript knockdown in Bombus terrestris, following ingestion of pest-specific dsRNA
Taning, C. N. T., Gui, S., Schutter, K. D., Jahani, M., Castellanos, N. L., Christiaens, O., & Smagghe, G. J. (2020) · Journal of Pest Science · doi:10.1007/s10340-020-01273-z · Cited by 43
A highly accumulated secretory protein from cotton bollworm interacts with basic helix–loop–helix transcription factor s to dampen plant defense
Chen, X., Liu, Y., Wu, M., Yan, L., Chen, C., Mu, Y., Liu, Y., Wang, M., Chen, X., & Mao, Y. (2022) · New Phytologist · doi:10.1111/nph.18507 · Cited by 42
Metal–Organic Framework-Based Insecticide and dsRNA Codelivery System for Insecticide Resistance Management
Yu, C., Li, J., Zhang, Z., et al. (2023) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.3c09074 · Cited by 43
Core RNAi machinery and gene knockdown in the emerald ash borer ( Agrilus planipennis )
Zhao, C., Gonzales, M. A. A., Poland, T. M., et al. (2014) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2014.12.002 · Cited by 43
“For example, using plant-mediated RNAi to silence expression of a cotton bollworm (Helicoverpa zea, Lepidoptera: Noctuidae) P450 monooxygenase gene has been shown to impair larval tolerance of gossypol (Mao et al., 2007).”
Background
Advances in RNA Interference Technology and Its Impact on Nutritional Improvement, Disease and Insect Control in Plants
Katoch, R., & Thakur, N. (2013) · Applied Biochemistry and Biotechnology · doi:10.1007/s12010-012-0046-5 · Cited by 43
Functional Analysis of Esterase TCE2 Gene from Tetranychus cinnabarinus (Boisduval) involved in Acaricide Resistance
Shi, L., Peng, W., Wang, X., et al. (2016) · Scientific Reports · doi:10.1038/srep18646 · Cited by 43
“RNAi has been successfully used to investigate the function of esterases, P450s, and GSTs in some insects, such as Aphis gossypii 23 , Sitobion avenae 24 , Helicoverpa armigera 22 , and Bemisia tabaci 25 .”
The overexpression of insect endogenous small RNAs in transgenic rice inhibits growth and delays pupation of striped stem borer ( Chilo suppressalis )
Jiang, S., Wu, H., Liu, H., Zheng, J., Lin, Y., & Chen, H. (2016) · Pest Management Science · doi:10.1002/ps.4477 · Cited by 43
Enhancing RNAi by using concatemerized double‐stranded RNA
Chandra, G. S., Asokan, R., Manamohan, M., & Kumar, N. K. (2018) · Pest Management Science · doi:10.1002/ps.5149 · Cited by 46
Regulation of mammalian gene expression by exogenous microRNAs
Liang, H., Huang, L., Cao, J., Zen, K., Chen, X., & Zhang, C. (2012) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1127 · Cited by 42
Physiological responses of emerald ash borer larvae to feeding on different ash species reveal putative resistance mechanisms and insect counter-adaptations
Rigsby, C. M., Showalter, D. N., Herms, D. A., Koch, J. L., Bonello, P., & Cipollini, D. F. (2015) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2015.05.001 · Cited by 42
“The substantially higher CAT activity observed in Mf larvae relative to susceptible hosts is suggestive that the H2O2 accumulation or production is greater in Manchurian ash.”
MethodInfluential
Corn rootworm-active RNA DvSnf7: Repeat dose oral toxicology assessment in support of human and mammalian safety
Petrick, J. S., Frierdich, G. E., Carleton, S. M., Kessenich, C. R., Silvanovich, A., Zhang, Y., & Koch, M. S. (2016) · Regulatory Toxicology and Pharmacology · doi:10.1016/j.yrtph.2016.07.009 · Cited by 44
RNA interference and crop protection against biotic stresses
Kaur, R., Choudhury, A., Chauhan, S., et al. (2021) · Physiology and Molecular Biology of Plants · doi:10.1007/s12298-021-01064-5 · Cited by 42
Over-expression of multiple cytochrome P450 genes in fenvalerate-resistant field strains of Helicoverpa armigera from north of China
Xu, L., Li, D., Qin, J., et al. (2016) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2016.01.003 · Cited by 42
Interaction of plant defense compounds with the insect gut: new insights from genomic and molecular analyses
Howe, G. A., & Herde, M. (2015) · Current Opinion in Insect Science · doi:10.1016/j.cois.2015.03.004 · Cited by 41
Knockdown of RNA Interference Pathway Genes in Western Corn Rootworms (Diabrotica virgifera virgifera Le Conte) Demonstrates a Possible Mechanism of Resistance to Lethal dsRNA
Vélez, A. M., Khajuria, C., Wang, H., Narva, K. E., & Siegfried, B. D. (2016) · PLoS ONE · doi:10.1371/journal.pone.0157520 · Cited by 42
“A number of recent studies have demonstrated that transgenic plants expressing insect-specific dsRNA can be effectively used to manage insect pest species [8–10].”
Background
Identification of Genes Potentially Responsible for extra-Oral Digestion and Overcoming Plant Defense from Salivary Glands of the Tarnished Plant Bug (Hemiptera: Miridae) Using cDNA Sequencing
Zhu, Y. C., Yao, J., & Luttrell, R. G. (2016) · Journal of Insect Science · doi:10.1093/jisesa/iew041 · Cited by 41
Expression of the double‐stranded RNA of the soybean pod borer Leguminivora glycinivorella (Lepidoptera: Tortricidae) ribosomal protein P0 gene enhances the resistance of transgenic soybean plants
Meng, F., Li, Y., Zang, Z., et al. (2017) · Pest Management Science · doi:10.1002/ps.4637 · Cited by 41
“4 DISCUSSION Several recent studies have examined the utility of RNAi techniques for controlling insect pests of agriculturally important crops.(7,13,14,15,16,23) The success of these studies suggests that RNAi-mediated crop protection is feasible.”
Background
Plant allelochemicals affect tolerance of polyphagous lepidopteran pest Helicoverpa armigera (Hübner) against insecticides
Chen, S., Elzaki, M. E. A., Ding, C., et al. (2018) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2018.12.009 · Cited by 41
RNAi targeting ecdysone receptor blocks the larva to adult development of Tetranychus cinnabarinus
Shen, G., Chen, W., Li, C.-Z., et al. (2019) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2019.05.020 · Cited by 41
Mechanism of plant–microbe interaction and its utilization in disease-resistance breeding for modern agriculture
Li, Y., Huang, F., Lu, Y., et al. (2013) · Physiological and Molecular Plant Pathology · doi:10.1016/j.pmpp.2013.05.001 · Cited by 41
New Insights on the Integrated Management of Plant Diseases by RNA Strategies: Mycoviruses and RNA Interference
Bocos‐Asenjo, I. T., Sánchez, J. N., Ginésy, M., & Díez, J. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23169236 · Cited by 45
“This was followed by work on insects: the growth of cotton bollworm larvae was successfully inhibited when fed leaves of transgenic plants expressing dsRNAs to silence their cytochrome P450 gene [141]; significant protection against western corn rootworm was achieved by in planta expression of gene-silencing dsRNAs [1…”
Background
Use of RNAi for Control of Insect Crop Pests
Swevers, L., & Smagghe, G. J. (2012) · Springer eBooks · doi:10.1007/978-94-007-3873-7_7 · Cited by 41
MicroRNA‐dependent development revealed by RNA interference‐mediated gene silencing of LmDicer1 in the migratory locust
Wang, Y., Yang, M., Jiang, F., et al. (2012) · Insect Science · doi:10.1111/j.1744-7917.2012.01542.x · Cited by 41
“A great success has recently been achieved by using the RNAi to silence essential genes for controlling growth and development of insects (Baum et al., 2007; Mao et al., 2007).”
Background
Biotechnology and Solutions: Insect-Pest-Resistance Management for Improvement and Development of Bt Cotton (Gossypium hirsutum L.)
Razzaq, A., Zafar, M. M., Ali, A., Li, P., Qadir, F., Zahra, L. T., Shaukat, F., Laghari, A. H., Yuán, Y., & Gǒng, W. (2023) · Plants · doi:10.3390/plants12234071 · Cited by 40
“When larvae were fed with such transgenic plant tissues expressing this double-stranded RNA construct, the transcription of this key cypP6AE14 gene in midgut cells of the pests was silenced, leading to retarded larvae growth due to the gossypol intoxication produced by the cotton plants [157].”
Background
A COMPLEX OF GENES INVOLVED IN ADAPTATION OF Leptinotarsa decemlineata LARVAE TO INDUCED POTATO DEFENSE
Petek, M., Turnšek, N., Gašparič, M. B., et al. (2012) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.21017 · Cited by 40
Biotechnological Approaches for the Control of Insect Pests in Crop Plants
Stevens, J., Dunse, K., Fox, J., Evans, S. C., & Anderso, M. (2012) · InTech eBooks · doi:10.5772/46233 · Cited by 40
RNA interference-mediated knockdown of IAP in Lygus lineolaris induces mortality in adult and pre-adult life stages
Walker, W. B., & Allen, M. L. (2010) · Entomologia Experimentalis et Applicata · doi:10.1111/j.1570-7458.2010.01078.x · Cited by 40
Construction of a genomewide RNA i mutant library in rice
Wang, L., Zheng, J., Luo, Y., Xu, T., Zhang, Q., Zhang, L., Xu, M., Wan, J., Wang, M., Zhang, C., et al. (2013) · Plant Biotechnology Journal · doi:10.1111/pbi.12093 · Cited by 40
“In plants, however, shRNA constructs have not proven to be highly effective; instead, long hpRNA transgenes have been widely used to induce gene silencing or confer virus resistance (Mao et al., 2007; Wang and Waterhouse, 2002), with the frequency of silencing often reaching >70% in a transgenic population (Smith et a…”
Background
Control of brown patch (Rhizoctonia solani) in tall fescue (Festuca arundinacea Schreb.) by host induced gene silencing
Zhou, B., Bailey, A. M., Niblett, C. L., et al. (2016) · Plant Cell Reports · doi:10.1007/s00299-015-1921-7 · Cited by 40
“The larvae fed with CYP6AE14derived hairpin (hpRNA) transgenic cotton showed reduced expression of CYP6AE14 and retarded growth (Mao et al. 2007).”

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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