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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Feeding‐based RNA interference of a trehalose phosphate synthase gene in the brown planthopper, Nilaparvata lugens
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“…al., 1998), scientists have explored a variety of efficient means to transport double-stranded RNA (dsRNA) into organisms, including microinjection, soaking, oral feeding and transgenic plant expression (Eaton et al., 2002; Baum et al., 2007; Mao et al., 2007; Chen et al., 2008; Tian et al., 2009).”
Background
Nematode resistance
Fuller, V. L., Lilley, C. J., & Urwin, P. E. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2008.02508.x · Cited by 249
New wind in the sails: improving the agronomic value of crop plants through RNA i‐mediated gene silencing
Koch, A., & Kogel, K. (2014) · Plant Biotechnology Journal · doi:10.1111/pbi.12226 · Cited by 248
“Through genetic and biochemical analyses, CYTOCHROME P450 (CYP6AE14) expression in the midgut of cotton bollworm (Helicoverpa armigera) larvae was found to be essential for tolerance to the cotton phytotoxin gossypol (Mao et al., 2007).”
Background
Biotic and Abiotic Constraints in Mungbean Production—Progress in Genetic Improvement
Nair, R. M., Pandey, A. K., War, A. R., HanumanthaRao, B., Shwe, T., Alam, A., Pratap, A., Malik, S. R., Karimi, R., Mbeyagala, E. K., et al. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.01340 · Cited by 237
“RNAi technology has been used against a number of insect-pests such as H. armigera by targeting the CYP6AE14 gene 9 (Mao et al., 2007).”
Method
RNA interference in the termite Reticulitermes flavipes through ingestion of double-stranded RNA
Zhou, X. J., Wheeler, M. M., Oi, F. M., & Scharf, M. E. (2008) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2008.05.005 · Cited by 235
“Plant-mediated RNAi has recently been demonstrated as a viable approach for control of phytophagous insect pests in agricultural settings (Baum et al., 2007; Mao et al., 2007).”
Background
Ineffective delivery of diet-derived microRNAs to recipient animal organisms
Snow, J. W., Hale, A., Isaacs, S. K., Baggish, A. L., & Chan, S. Y. (2013) · RNA Biology · doi:10.4161/rna.24909 · Cited by 238
Host‐induced post‐transcriptional hairpin RNA ‐mediated gene silencing of vital fungal genes confers efficient resistance against F usarium wilt in banana
Ghag, S. B., Shekhawat, U. K. S., & Ganapathi, T. R. (2014) · Plant Biotechnology Journal · doi:10.1111/pbi.12158 · Cited by 229
RNA-based technologies for insect control in plant production
Liu, S., Jaouannet, M., Dempsey, D. A., Imani, J., Coustau, C., & Kogel, K. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.107463 · Cited by 235
Crop Improvement Through Temperature Resilience
Zhang, J., Li, X., Lin, H., & Chong, K. (2019) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-100016 · Cited by 225
Cross-kingdom RNA trafficking and environmental RNAi — nature's blueprint for modern crop protection strategies
Cai, Q., He, B., Kogel, K., & Jin, H. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2018.02.003 · Cited by 236
Biotechnological Prospects for Engineering Insect-Resistant Plants
Gatehouse, J. A. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.111096 · Cited by 217
New insights into an RNAi approach for plant defence against piercing‐sucking and stem‐borer insect pests
Li, H., Guan, R., Guo, H., et al. (2015) · Plant Cell & Environment · doi:10.1111/pce.12546 · Cited by 217
“Current dsRNA treatment modes (microinjection, spraying and/or feeding) are particularly popular and appear to be feasible for insects (Araujo et al. 2006; Turner et al. 2006; Baum et al. 2007; Mao et al. 2007; Wang et al. 2011).”
Background
Melatonin enhances cotton immunity to Verticillium wilt via manipulating lignin and gossypol biosynthesis
Li, C., He, Q., Zhang, F., Yu, J., Li, C., Zhao, T., Zhang, Y., Xie, Q., Su, B., Mei, L., et al. (2019) · The Plant Journal · doi:10.1111/tpj.14477 · Cited by 217
“All the amino acid sequences were checked against Pfam (http://pfam.sanger.ac.uk/) (Finn et al., 2014) and the NCBI Conserved Domain Database (http://www.ncbi.nlm.nih. gov/cdd) (Marchler-Bauer et al., 2015) to confirm the conserved domains.”
Method
Feasibility, limitation and possible solutions of RNAi‐based technology for insect pest control
Zhang, H., Li, H., & Miao, X. (2012) · Insect Science · doi:10.1111/j.1744-7917.2012.01513.x · Cited by 229
“Mao et al. (2007) constructed a cDNA library from RNAs expressed in the midgut of fifth-instar larvae exposed to gossypol, and identified several gossypol inducible genes, which contained a putative P450 monooxygenase, CYP6AE14 (Mao et al., 2007).”
BackgroundMethodInfluential
Genomics of adaptation to host-plants in herbivorous insects
Simon, J., d’Alençon, E., Guy, E., Jacquin‐Joly, E., Jaquiéry, J., Nouhaud, P., Peccoud, J., Sugio, A., & Streiff, R. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv015 · Cited by 226
“ance to gossypol [91].”
RNA Interference in Insects: Protecting Beneficials and Controlling Pests
Vogel, E., Santos, D., Mingels, L., Verdonckt, T.-W., & Broeck, J. V. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2018.01912 · Cited by 228
“In this research, Mao et al. (2007) showed that plantmediated expression of dsRNA targeting the cytochrome P450 monooxygenase gene (CYP6AE14) could increase the toxic effects of gossypol, a cotton metabolite that is otherwise tolerated by the cotton bollworm.”
Background
A nuclease specific to lepidopteran insects suppresses RNAi
Guan, R., Li, H., Fan, Y., Hu, S., Christiaens, O., Smagghe, G. J., & Miao, X. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.001553 · Cited by 223
Host‐induced gene silencing: a tool for understanding fungal host interaction and for developing novel disease control strategies
Nunes, C. C., & Dean, R. A. (2011) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2011.00766.x · Cited by 201
“For other examples, see Mao et al., 2007; Turner et al., 2006.”
BackgroundMethod
Environmental Fate of RNA Interference Pesticides: Adsorption and Degradation of Double-Stranded RNA Molecules in Agricultural Soils
Parker, K. M., Barragán‐Borrero, V., van Leeuwen, D., Lever, M. A., Mateescu, B., & Sander, M. (2019) · Environmental Science & Technology · doi:10.1021/acs.est.8b05576 · Cited by 211
Second-Generation Sequencing Supply an Effective Way to Screen RNAi Targets in Large Scale for Potential Application in Pest Insect Control
Wang, Y., Zhang, H., Li, H., & Miao, X. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018644 · Cited by 195
“In addition, two research papers indicate that transgenic crops can produce dsRNAs to protect the plant against insect feeding damage [16,17].”
Background
RNA interference in Colorado potato beetle: steps toward development of dsRNA as a commercial insecticide
Palli, S. R. (2014) · Current Opinion in Insect Science · doi:10.1016/j.cois.2014.09.011 · Cited by 197
Application of RNA silencing to plant disease resistance
Duan, C., Wang, C., & Guo, H. (2012) · Silence · doi:10.1186/1758-907x-3-5 · Cited by 196
Genetic basis for glandular trichome formation in cotton
Ma, D., Hu, Y., Yang, C., et al. (2016) · Nature Communications · doi:10.1038/ncomms10456 · Cited by 196
Selection and Evaluation of Potential Reference Genes for Gene Expression Analysis in the Brown Planthopper, Nilaparvata lugens (Hemiptera: Delphacidae) Using Reverse-Transcription Quantitative PCR
Yuan, M., Lu, Y., Zhu, X., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086503 · Cited by 193
“At present, RNA interference (RNAi) is an effective tool to control important insect pests via gene silencing [9,10,11,12,13].”
Background
Phloem sap intricacy and interplay with aphid feeding
Dinant, S., Bonnemain, J., Girousse, C., et al. (2010) · Comptes Rendus Biologies · doi:10.1016/j.crvi.2010.03.008 · Cited by 191
Insect Detoxification and Sequestration Strategies
Heckel, D. G. (2014) · doi:10.1002/9781118829783.ch3 · Cited by 191
Genetically Engineered Plants and Foods: A Scientist's Analysis of the Issues (Part II)
Lemaux, P. G. (2009) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.043008.092013 · Cited by 193
“As insect resistance to Cry toxins currently deployed in Bt crops increases, other strategies to create GE crops resistant to insects are being developed, including vegetative insecticidal proteins (Vips) from Bt (190) and RNA interference (RNAi) (32, 195).”
Background
RNA Silencing in Plants: Mechanisms, Technologies and Applications in Horticultural Crops
Guo, Q., Liu, Q., Smith, N. A., Liang, G., & Wang, M. (2016) · Current Genomics · doi:10.2174/1389202917666160520103117 · Cited by 190
“Transgenic tobacco plants expressing hpRNA directed against CYP6AE14 was shown to provide sufficient levels of specific dsRNA to suppress gene expression in the insect midgut [98].”
Background
Enhanced Whitefly Resistance in Transgenic Tobacco Plants Expressing Double Stranded RNA of v-ATPase A Gene
Thakur, N., Upadhyay, S. K., Verma, P. C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087235 · Cited by 189
“Transgenic plant-mediated delivery of dsRNA in the insect gut may cause a wide range of disturbances in insect physiology, ranging from moulting defects to death [23,24,25].”
BackgroundInfluential
RNA Interference (RNAi) Induced Gene Silencing: A Promising Approach of Hi-Tech Plant Breeding
Younis, A., Siddique, M. I., Kim, C.-K., & Lim, K. (2014) · International Journal of Biological Sciences · doi:10.7150/ijbs.10452 · Cited by 190
“A gene ‘CYP6AE14’ was identified in Helicoverpa armigera [26].”
BackgroundInfluential
Interplay between insects and plants: dynamic and complex interactions that have coevolved over millions of years but act in milliseconds
Bruce, T. J. A. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru391 · Cited by 189
“For example, cotton bollworm (Helicoverpa armigera) uses a P450, CYP6AE14, to detoxify gossypol (Mao et al., 2007); hawkmoth can feed on O-acyl-sugar-producing N.”
Background
An effector from cotton bollworm oral secretion impairs host plant defense signaling
Chen, C., Liu, Y.-Q., Song, W.-M., Chen, D.-Y., Chen, F., Chen, X., Chen, Z., Ge, S., Wang, C., Zhan, S., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1905471116 · Cited by 189
Induction of Systemic Resistance against Insect Herbivores in Plants by Beneficial Soil Microbes
Rashid, M. H.-O., & Chung, Y. R. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01816 · Cited by 194
“LOX has a prominent and direct role in stimulating plant defense by producing protease inhibitors and oxidative enzymes (Mao et al., 2007).”
Background
Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Diaphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing)
Hajeri, S., Killiny, N., El-Mohtar, C. A., Dawson, W. O., & Gowda, S. (2014) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2014.02.010 · Cited by 184
Small RNAs — the secret agents in the plant–pathogen interactions
Weiberg, A., & Jin, H. (2015) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2015.05.033 · Cited by 193
Saliva of Lygus lineolaris digests double stranded ribonucleic acids
Allen, M. L., & Walker, W. B. (2011) · Journal of Insect Physiology · doi:10.1016/j.jinsphys.2011.12.014 · Cited by 178
“For pest control, the idea of incorporating dsRNA into plants to combat insects has been proposed (Baum et al., 2007; Gordon and Waterhouse, 2007; Mao et al., 2007; Whyard et al., 2009).”
Background
Safe nanotechnologies for increasing the effectiveness of environmentally friendly natural agrochemicals
Vurro, M., Miguel‐Rojas, C., & Pérez‐de‐Luque, A. (2019) · Pest Management Science · doi:10.1002/ps.5348 · Cited by 177

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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