Silencing a cotton bollworm P450 monooxygenase gene by plant-mediated RNAi impairs larval tolerance of gossypol
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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The potential of RNAi for pest control was first demonstrated in 2007 for H. armigera and Diabrotica virgifera virgifera.
“The potential of RNAi for pest control has first been demonstrated in 2007 for H. armigera and Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) (Baum et al., 2007;Mao et al., 2007).”
From Genetically engineered crops help support conservation biological control (2019) · cites this paper as Mao et al., 2007
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“Transgenic plants Transgenic crops expressing dsRNA/siRNA have a number of advantages in pest management (Mao et al., 2007).”
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Kamthan, A., Chaudhuri, A., Kamthan, M., & Datta, A. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00208 · Cited by 305 · see citing works
“Cotton bollworm (Helicoverpa armigera) larvae showed reduced growth when fed on plant material expressing dsRNA specific to cytochrome P450 gene (CYP6AE14; Mao et al., 2007).”
MethodA Perspective on RNAi-Based Biopesticides
Fletcher, S. J., Reeves, P. T., Hoang, L. B. T., & Mitter, N. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.00051 · Cited by 302 · see citing works
Insect Response to Plant Defensive Protease Inhibitors
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Control of cotton fibre elongation by a homeodomain transcription factor GhHOX3
Shan, C., Shangguan, X., Zhao, B., Zhang, X., Chao, L., Yang, C., Wang, L., Zhu, H.-Y., Zeng, Y.-D., Wang-Zhen, G. U. O., et al. (2014) · Nature Communications · doi:10.1038/ncomms6519 · Cited by 296 · see citing works
Insect-Resistant Genetically Modified Rice in China: From Research to Commercialization
Chen, M., Shelton, A. M., & Yè, G. (2010) · Annual Review of Entomology · doi:10.1146/annurev-ento-120709-144810 · Cited by 290 · see citing works
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“, 2006) to silence a gut carboxylesterase and a pheromone binding protein gene; and plants expressing short hairpin dsRNA feeding to Helicoverpa armigera (Mao et al., 2007) to silence a P450 gene involved in gossypol tolerance.”
BackgroundInfluentialYan, S., Qian, J., Cai, C., Ma, Z., Li, J., Yin, M., Ren, B., & Shen, J. (2019) · Journal of Pest Science · doi:10.1007/s10340-019-01157-x · Cited by 282 · see citing works
Regulation of Midgut Growth, Development, and Metamorphosis
Hakim, R. S., Baldwin, K. M., & Smagghe, G. J. (2009) · Annual Review of Entomology · doi:10.1146/annurev-ento-112408-085450 · Cited by 279 · see citing works
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“Two breakthrough reports demonstrated that insects feeding on transgenic plants engineered to produce specific double-stranded dsRNA resulted in the suppression of target gene expression in the cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) (Mao et al.”
BackgroundLack of detectable oral bioavailability of plant microRNAs after feeding in mice
Dickinson, B., Zhang, Y., Petrick, J. S., Heck, G. R., Ivashuta, S. I., & Marshall, W. S. (2013) · Nature Biotechnology · doi:10.1038/nbt.2737 · Cited by 273 · see citing works
Cotton plants expressing CYP6AE14 double-stranded RNA show enhanced resistance to bollworms
Mao, Y., Tao, X., Xue, X., Wang, L.-J., & Chen, X. (2010) · Transgenic Research · doi:10.1007/s11248-010-9450-1 · Cited by 263 · see citing works
“Construction of vectors and cotton plant transformation The dsRNA construct pBI121-dsCYP6AE14 as described by Mao et al. (2007) contained a 35S promoter, a sense fragment of CYP6AE14 complementary DNA (cDNA) from ?”
BackgroundInfluentialEnvironmental RNA interference
Whangbo, J., & Hunter, C. P. (2008) · Trends in Genetics · doi:10.1016/j.tig.2008.03.007 · Cited by 257 · see citing works
How to cope with insect resistance to Bt toxins?
Bravo, A., & Soberón, M. (2008) · Trends in biotechnology · doi:10.1016/j.tibtech.2008.06.005 · Cited by 255 · see citing works
Mao, Y., Liu, Y.-Q., Chen, D.-Y., Chen, F., Fang, X., Hong, G., Wang, L.-J., Wang, J., & Chen, X. (2017) · Nature Communications · doi:10.1038/ncomms13925 · Cited by 256 · see citing works
P450s in plant–insect interactions
Schuler, M. A. (2010) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2010.09.012 · Cited by 252 · see citing works
RNA interference for the control of whiteflies (Bemisia tabaci) by oral route
Upadhyay, S. K., Chandrashekar, K., Thakur, N., Verma, P. C., Borgio, J. F., Singh, P. K., & Tuli, R. (2011) · Journal of Biosciences · doi:10.1007/s12038-011-9009-1 · Cited by 249 · see citing works
“Mao et al. (2007) and Baum et al. (2007) have demonstrated that the physiology of the insects can be disturbed with siRNA, which generally leads to the reduction in larval growth and sometimes death.”
BackgroundRNA interference: concept to reality in crop improvement
Saurabh, S., Vidyarthi, A. S., & Prasad, D. (2014) · Planta · doi:10.1007/s00425-013-2019-5 · Cited by 252 · see citing works
RNAi technology: a new platform for crop pest control
Mamta, B., & Rajam, M. V. (2017) · Physiology and Molecular Biology of Plants · doi:10.1007/s12298-017-0443-x · Cited by 246 · see citing works
“As a result, larvae were not able to detoxify gossypol and showed retarded growth (Mao et al. 2007).”
BackgroundMethodInfluentialBachman, P. M., Bolognesi, R., Moar, W. J., Mueller, G. M., Paradise, M. S., Ramaseshadri, P., Tan, J., Uffman, J. P., Warren, J., Wiggins, B. E., et al. (2013) · Transgenic Research · doi:10.1007/s11248-013-9716-5 · Cited by 242 · see citing works
“Transgenic crops have been developed to express insecticidal dsRNAs and offer a new approach for agricultural pest control (Baum et al. 2007; Mao et al. 2007).”
BackgroundGenetically engineered crops help support conservation biological control
Romeis, J., Naranjo, S. E., Meissle, M., & Shelton, A. M. (2019) · Biological Control · doi:10.1016/j.biocontrol.2018.10.001 · Cited by 231 · see citing works
“The potential of RNAi for pest control has first been demonstrated in 2007 for H. armigera and Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) (Baum et al., 2007; Mao et al., 2007).”
BackgroundChen, J., Zhang, D., Yao, Q., et al. (2010) · Insect Molecular Biology · doi:10.1111/j.1365-2583.2010.01038.x · Cited by 238 · see citing works
“…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).”
BackgroundFuller, V. L., Lilley, C. J., & Urwin, P. E. (2008) · New Phytologist · doi:10.1111/j.1469-8137.2008.02508.x · Cited by 238 · see citing works
Koch, A., & Kogel, K. (2014) · Plant Biotechnology Journal · doi:10.1111/pbi.12226 · Cited by 237 · see citing works
“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).”
BackgroundBiotic 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 · see citing works
“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).”
MethodRNA 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 230 · see citing works
“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).”
BackgroundIneffective 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 235 · see citing works
Ghag, S. B., Shekhawat, U. K. S., & Ganapathi, T. R. (2014) · Plant Biotechnology Journal · doi:10.1111/pbi.12158 · Cited by 229 · see citing works
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 229 · see citing works
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 224 · see citing works
Cai, Q., He, B., Kogel, K., & Jin, H. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2018.02.003 · Cited by 223 · see citing works
Biotechnological Prospects for Engineering Insect-Resistant Plants
Gatehouse, J. A. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.111096 · Cited by 217 · see citing works
Li, H., Guan, R., Guo, H., et al. (2015) · Plant Cell & Environment · doi:10.1111/pce.12546 · Cited by 217 · see citing works
“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).”
BackgroundLi, 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 216 · see citing works
“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.”
MethodFeasibility, 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 217 · see citing works
“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).”
BackgroundMethodInfluentialGenomics of adaptation to host-plants in herbivorous insects
Simon, J., d’Alençon, E., Guy, E., et al. (2015) · Briefings in Functional Genomics · doi:10.1093/bfgp/elv015 · Cited by 216 · see citing works
“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 216 · see citing works
“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.”
BackgroundA nuclease specific to lepidopteran insects suppresses RNAi
Guan, R., Li, H., Fan, Y., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.001553 · Cited by 215 · see citing works
Nunes, C. C., & Dean, R. A. (2011) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2011.00766.x · Cited by 201 · see citing works
“For other examples, see Mao et al., 2007; Turner et al., 2006.”
BackgroundMethodParker, 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 201 · see citing works
Wang, Y., Zhang, H., Li, H., & Miao, X. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018644 · Cited by 195 · see citing works
“In addition, two research papers indicate that transgenic crops can produce dsRNAs to protect the plant against insect feeding damage [16,17].”
BackgroundPalli, S. R. (2014) · Current Opinion in Insect Science · doi:10.1016/j.cois.2014.09.011 · Cited by 197 · see citing works
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 · see citing works
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 · see citing works
Yuan, M., Lu, Y., Zhu, X., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0086503 · Cited by 193 · see citing works
“At present, RNA interference (RNAi) is an effective tool to control important insect pests via gene silencing [9,10,11,12,13].”
BackgroundPhloem 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 · see citing works
Insect Detoxification and Sequestration Strategies
Heckel, D. G. (2014) · doi:10.1002/9781118829783.ch3 · Cited by 191 · see citing works
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 190 · see citing works
“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).”
BackgroundRNA 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 · see citing works
“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].”
BackgroundThakur, N., Upadhyay, S. K., Verma, P. C., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0087235 · Cited by 189 · see citing works
“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].”
BackgroundInfluentialRNA 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 · see citing works
“A gene ‘CYP6AE14’ was identified in Helicoverpa armigera [26].”
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“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.”
BackgroundAn effector from cotton bollworm oral secretion impairs host plant defense signaling
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Induction of Systemic Resistance against Insect Herbivores in Plants by Beneficial Soil Microbes
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“LOX has a prominent and direct role in stimulating plant defense by producing protease inhibitors and oxidative enzymes (Mao et al., 2007).”
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Small RNAs — the secret agents in the plant–pathogen interactions
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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 · see citing works
“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).”
BackgroundVurro, M., Miguel‐Rojas, C., & Pérez‐de‐Luque, A. (2019) · Pest Management Science · doi:10.1002/ps.5348 · Cited by 177 · see citing works
- 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
- Venue
- Nature Biotechnology
- Published
- 2007-11
- Volume
- 25
- Issue
- 11
- Pages
- 1307-1313
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- 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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