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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 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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“…RNAi strategy Expression in transgenic plants of double strand (dsRNA) designed against insect target genes has been shown to give protection against pests through RNA interference (RNAi), opening the way for a new generation of insectresistant crops (Baum et al. 2007; Mao et al. 2007; Price Fig.”
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“Insect genes can be knocked down, rather than knocked out, by the microinjection of dsRNA [4,28,29], the uptake of exogenous dsRNA from an artificial diet [5], or through plant-mediated strategies [1,2,6].”
InfluentialPeng, W., Li, J., Liu, X., Nan, C., Shi, L., Zhang, Y., Li, C., & He, L. (2018) · Pest Management Science · doi:10.1002/ps.5109 · Cited by 63
Plant-Mediated RNAi for Controlling Apolygus lucorum
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“In 2007, the first plant-mediated RNAi was applied on cotton, which expressed dsRNA specific to a cytochrome P450 gene (CYP6AE14), for the control the cotton bollworm, Helicoverpa armigera (Mao et al., 2007).”
BackgroundMethodBento, F. D. M. M., Marques, R. N., Campana, F. B., et al. (2019) · Pest Management Science · doi:10.1002/ps.5513 · Cited by 62
Dietary RNAi toxicity assay exhibits differential responses to ingested dsRNAs among lady beetles
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Feeding-Based RNA Intereference of a Gap Gene Is Lethal to the Pea Aphid, Acyrthosiphon pisum
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“dsRNA can be delivered to insects through oral feeding, microinjection, soaking and transgenic expression [6,9,12,30,31,32,33].”
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“In planta, the expression of dsRNAs that cause the knockdown of functional genes in chewing insects provides a new avenue for environmentally-friendly pest management [43,57].”
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“Recent applications of RNAi in crops include corn and cotton plants resistant to insect pests (Baum et al., 2007; Mao et al., 2007; Price and Gatehouse, 2008) and soybeans resistant to root-knot nematodes (Huang et al., 2006).”
BackgroundSuppression of Bedbug’s Reproduction by RNA Interference of Vitellogenin
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Chemical mediation as a structuring element in marine gastropod predator-prey interactions
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The advent of RNA interference in Entomology
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“Meyering-Vos and Müller (2007) found that treatment of the adult cricket, G.”
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“RNAi has also been proposed as a potential approach to insect pest control (Baum et al., 2007; Mao et al., 2007; Price & Gatehouse, 2008); however, although the response to RNAi has been reported in the orders of Hymenoptera, Diptera, Coleoptera, Lepidoptera, Hemiptera, Dictyoptera, Isoptera and Orthoptera, the sensit…”
BackgroundThe humanitarian impact of plant biotechnology: recent breakthroughs vs bottlenecks for adoption
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“In addition to chemical applications, chitin synthase genes could be targeted through an RNA-interference (RNAi) based approach [47-48].”
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Zhou, G., Zhou, Y., & Chen, X. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00768 · Cited by 61
“For example, transgenic plants engineered to produce dsRNAs against essential pest genes were more resistant to pest attack (Mao et al., 2007).”
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Plant‐mediated RNAi of grain aphid CHS1 gene confers common wheat resistance against aphids
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How many genetic options for evolving insecticide resistance in heliothine and spodopteran pests?
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Cysteine protease enhances plant-mediated bollworm RNA interference
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“Keywords Cysteine proteases Peritrophic matrix Helicoverpa armigera Gossypol RNAi Insect control”
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Gene silencing in adult Aedes aegypti mosquitoes through oral delivery of double‐stranded RNA
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“…Hymenoptera (Aronstein et al. 2006; Nunes and Simoes 2009), Isoptera (Zhou et al. 2008), Lepi-doptera (Rajagopal et al. 2002; Turner et al. 2006; Mao et al. 2007; Griebler et al. 2008; Bautista et al. 2009; Kumar et al. 2009; Tian et al. 2009; Whyard et al. 2009) and Orthoptera (Meyering-Vos…”
RNA Interference for Functional Genomics and Improvement of Cotton (Gossypium sp.)
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“The expression of CYP9A subfamily and CYP6AE14 genes can be induced by gossypol [12, 15].”
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RetractedRisk assessment of RNAi-based biopesticides
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“Given the specificity of RNAi technology, its use in transgenic plants expressing hairpin RNAs designed to suppress vital genes in specific insect pests upon ingestion offers a new approach to managing crop pests (Baum et al. 2007; Mao et al. 2007).”
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Tyrosine Metabolism for Insect Cuticle Pigmentation and Sclerotization
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“Plant-mediated dsRNA delivery has been shown to be an effective way to silence target genes in lepidopterans (Kumar et al., 2014; Mao et al., 2007; Poreddy et al., 2017; Poreddy et al., 2015; Zhang et al., 2017), for which dsRNA can be constantly incorporated by dietary ingestion.”
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“a severe retardation of larval growth [17].”
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Dietary Risk Assessment of v-ATPase A dsRNAs on Monarch Butterfly Larvae
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“…studies (Roberts et al., 2015; Xu et al., 2015), oral exposure of dsRNA by dietary RNAi is the most relevant delivery method for the development of novel control alternatives, either through transgenic plants, baits, or formulations (Baum et al., 2007; Mao et al., 2007; Xu et al., 2015).”
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“Gossypol, for example, is a well-known phytoanticipin in cotton and it has been shown that UGT-glycosylation and P450-oxygenation of gossypol are important for gossypol detoxification (Mao et al. 2007; Krempl et al. 2016).”
BackgroundGenome editing for resistance against plant pests and pathogens
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“armigera larvae were then fed with artificial feed containing gossypol, their growth and development were significantly inhibited (Mao et al., 2007).”
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Camargo, R. A., Herai, R. H., Santos, L. N., et al. (2015) · BMC Genomics · doi:10.1186/s12864-015-1841-5 · Cited by 56
“However, the demonstration that transgenic plants modified to express insect dsRNA can successfully control target pests [5, 6] raised the possibility of developing RNAi-mediated crop protection [3, 4, 7].”
BackgroundMolecular profiling — a tool for addressing emerging gaps in the comparative risk assessment of GMOs
Heinemann, J. A., Kurenbach, B., & Quist, D. (2011) · Environment International · doi:10.1016/j.envint.2011.05.006 · Cited by 56
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“Gene silencing has been achieved in various insect pests employing dsRNA corresponding to various genes encoding developmental proteins [22], salivary gland proteins involved in digestion [23, 24], gut enzymes [15], hormone receptors [25, 26], or even proteins involved in host-insect interaction [18, 27].”
BackgroundYan, N., Du, Y., Liu, X., et al. (2015) · Industrial Crops and Products · doi:10.1016/j.indcrop.2015.12.031 · Cited by 56
Diet-derived microRNAs: unicorn or silver bullet?
Witwer, K. W., & Zhang, C.-Y. (2017) · Genes & Nutrition · doi:10.1186/s12263-017-0564-4 · Cited by 57
Dissipation of double-stranded RNA in aquatic microcosms
Albright, V. C., Wong, C. R., Hellmich, R. L., & Coats, J. R. (2016) · Environmental Toxicology and Chemistry · doi:10.1002/etc.3648 · Cited by 55
Adaptive regulation of detoxification enzymes in Helicoverpa armigera to different host plants
Jin, M., Liao, C.-Y., Fu, X.-Z., et al. (2019) · Insect Molecular Biology · doi:10.1111/imb.12578 · Cited by 55
“Transcriptional studies showed that CYP6AE14 is highly upregulated in H. armigera larvae after gossypol feeding and that silencing of this gene leads to retarded growth in gossypol-fed larvae (Mao et al., 2007; Celorio-Mancera et al., 2011).”
BackgroundInfluentialZeng, X., Pan, Y., Tian, F., et al. (2021) · Pesticide Biochemistry and Physiology · doi:10.1016/j.pestbp.2021.104879 · Cited by 55
No impact of DvSnf7 RNA on honey bee ( Apis mellifera L.) adults and larvae in dietary feeding tests
Tan, J., Levine, S. L., Bachman, P. M., Jensen, P. D., Mueller, G. M., Uffman, J. P., Meng, C., Song, Z., Richards, K. B., & Beevers, M. H. (2015) · Environmental Toxicology and Chemistry · doi:10.1002/etc.3075 · Cited by 56
“Two important studies, 1 conducted using the western corn rootworm (Diabrotica virgifera virgifera) [6] and 1 with the cotton bollworm (Helicoverpa armigera) [7], demonstrated the practical application of RNA interference in insect pest control using sequence-specific gene silencing to suppress genes critical for inse…”
BackgroundBansal, R., & Michel, A. P. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms14023786 · Cited by 55
“glycines control using transgenic plants expressing RNAi [48,49].”
BackgroundHost-Pathogen interactions modulated by small RNAs
Islam, W., Islam, S. U., Qasim, M. U., & Wang, L. (2017) · RNA Biology · doi:10.1080/15476286.2017.1318009 · Cited by 54
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Evolution of Disease Defense Genes and Their Regulators in Plants
Zhang, R., Zheng, F., Wei, S., Zhang, S., Li, G., Cao, P., & Zhao, S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020335 · Cited by 59
“Transgene-derived artificial sRNAs in plants can induce the target gene silencing in certain interacting insects [84,85], nematodes [86], fungi [87–90], oomycetes [91,92], and even plants–plants [141].”
BackgroundXiao, T., & Lǚ, K. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.08.014 · Cited by 54
Cui, C., Wang, Y., Li, Y., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111527 · Cited by 54
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“For example, Mao et al. (2007) fed H. armigera larvae with plant material expressing double-stranded RNA (dsRNA) specific to CYP6AE14, successfully decreasing the transcripts of the target gene, and thus resulting in growth retardation.”
BackgroundNew Approaches to Agricultural Insect Pest Control Based on RNA Interference
Xue, X., Mao, Y., Tao, X., Huang, Y., & Chen, X. (2012) · Advances in insect physiology · doi:10.1016/b978-0-12-387680-5.00003-3 · Cited by 54
Metadata
- 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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