Genome mining and functional analysis of cytochrome P450 genes involved in insecticide resistance in <i>Leucinodes orbonalis</i> (Lepidoptera: Crambidae)

Kariyanna, B; Prabhuraj, A.; Asokan, R.; Ramkumar, Govindaraju; Venkatesan, T.; Gracy, R. Gandhi; Mohan, M.

doi:10.1002/bab.1997

Cited by 13 publications

(7 citation statements)

References 56 publications

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“…Notably, 20E biosynthesis gene CYP306A1 RNAi and in vitro metabolism have further confirmed that CYP306A1 is likely to be involved in the resistance to IMD. The potential role of 20E‐released genes in resistance to insecticide has also been found in other insects, including Aphid craccivora , 20 Chilo suppressalis 19 and Leucinodes orbonalis 51 . These results suggest that not only in the CYP3 and CYP4 families but also other P450s clans may have a function in insecticide resistance.…”

Section: Discussionsupporting

confidence: 52%

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

Liu

Zhang

et al. 2023

Pest Management Science

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BackgroundDifference in physiology level between the immature and mature stages of insects likely contribute to different mechanisms of insecticide resistance. It is well acknowledged that insect 20‐hydroxyecdysone (20E) plays an important role in many biological processes in the immature stage, whether 20E confers insecticide resistance at this specific stage is still poorly understood. By gene cloning, reverse transcription quantitative real‐time PCR, RNA interference (RNAi) and in vitro metabolism experiments, this study aimed to investigate the potential role of 20E‐related genes in conferring imidacloprid (IMD) resistance in the immature stage of the whitefly Bemisia tabaci Mediterranean.ResultsAfter identification of low to moderate IMD resistance in the whitefly, we found CYP306A1 of the six 20E‐related genes was overexpressed in the nymph stage of the three resistant strains compared to a laboratory reference susceptible strain, but not in the adult stage. Further exposure to IMD resulted in an increase in CYP306A1 expression in the nymph stage. These results together imply that CYP306A1 may be implicated in IMD resistance in the nymph stage of the whitefly. RNAi knockdown of CYP306A1 increased the mortality of nymphs after treatment with IMD in bioassay, suggesting a pivotal role of CYP306A1 in conferring IMD resistance in the nymph stage. Additionally, our metabolism experiments in vivo showed that the content of IMD reduced by 20% along with cytochrome P450 reductase and heterologously expressed CYP306A1, which provides additional evidence for the important function of CYP306A1 in metabolizing IMD that leads to the resistance.ConclusionThis study uncovers a novel function of the 20E biosynthesis gene CYP306A1 in metabolizing imidacloprid, thus contributing to such resistance in the immature stage of the insect. These findings not only advance our understanding of 20E‐mediated insecticide resistance, but also provide a new target for sustainable pest control of global insect pests such as whitefly. © 2023 Society of Chemical Industry.

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Section: Discussionsupporting

confidence: 52%

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

Liu

Zhang

et al. 2023

Pest Management Science

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“…In Anopheles gambiae, Apis mellifera, B. mori, D. melanogaster, Nasonia vitripennis, and T. castaneum respectively 28,8,23,37,19,35 GSTs and 51,24,76,35,41,49 CEs were identified (Yu et al, 2008(Yu et al, , 2009Oakeshott et al, 2010). Similarly, the gene expansion of cytochromoe p450 monooxygenases (CYP) and their role in insecticide resistance in L. orbonalis were recently documented (Kariyanna, 2019;Kariyanna et al, 2020a). Together with the results of present and earlier studies it is very much evident that multiple metabolic enzymes contribute toward overall insecticide resistance in L. orbonalis.…”

Section: Discussionmentioning

confidence: 95%

“…The enhanced detoxification of insecticides by metabolic enzymes viz., carboxylesterases (CE) and glutathione S-transferases (GSTs) are commonly reported in resistant populations of many insect species and mites (Ranson et al, 2002;Enayati et al, 2005;Oakeshott et al, 2005;Perry et al, 2011;Das and Dutta, 2014;Akıner and Ekşi, 2015;Benoit et al, 2015). The resistant individuals metabolize the insecticides faster due to higher catalytic rate or enhanced production of the enzyme as a consequence of increased transcription or gene duplication (Panini et al, 2016;Kariyanna et al, 2020a). The GSTs are phase II metabolic enzymes and are distributed in most of the animals (Hayes and Pulford, 1995).…”

Section: Introductionmentioning

confidence: 99%

Genome Mining and Expression Analysis of Carboxylesterase and Glutathione S-Transferase Genes Involved in Insecticide Resistance in Eggplant Shoot and Fruit Borer, Leucinodes orbonalis (Lepidoptera: Crambidae)

et al. 2020

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The shoot and fruit borer, Leucinodes orbonalis (Lepidoptera: Crambidae) is the major cause of low productivity in eggplant and insecticides being the mainstay of management of L. orbonalis. However, field control failures are widespread due to the evolution of insecticide resistance. Taking advantage of the whole genome sequence information, the present study investigated the level of insecticide resistance and the expression pattern of individual carboxylesterase (CE) and glutathione S-transferases (GSTs) genes in various field collected populations of L. orbonalis. Dose-mortality bioassays revealed a very high level of resistance development against fenvalerate (48.2–160-fold), phosalone (94-534.6-fold), emamectin benzoate (7.2–55-fold), thiodicarb (9.64–22.7-fold), flubendiamide (187.4–303.0-fold), and chlorantraniliprole (1.6–8.6-fold) in field populations as compared to laboratory-reared susceptible iso-female colony (Lo-S). Over-production of detoxification enzymes viz., CE and GST were evident upon enzyme assays. Mining of the draft genome of L. orbonalis yielded large number of genes potentially belonging to the CE and GST gene families with known history of insecticide resistance in other insects. Subsequent RT-qPCR studies on relative contribution of individual genes revealed over-expression of numerous GSTs and few CEs in field populations, indicating their possible involvement of metabolic enzymes in insecticide resistance. The genomic information will facilitate the development of novel resistance management strategies against this pest.

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“… Internal feeding in fruit with entry holes sealed make infested fruit difficult to detect unless cut open. Resistance to pesticides has developed within L. orbonalis (Ayam et al., 2016; Shirale et al., 2017; Kariyanna et al., 2020) driven by the frequent application of pesticides (e.g. there can be between 56 and 180 applications during the S. melongena growing season; Chakraborti and Senapati, 2016).…”

Section: Pest Categorisationmentioning

confidence: 99%

Pest categorisation of Leucinodes orbonalis

Bragard¹,

Serio²,

Gonthier³

et al. 2021

EFS2

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The EFSA Panel on Plant Health performed a pest categorisation of the eggplant fruit and shoot borer, Leucinodes orbonalis Guen ee, (Lepidoptera: Crambidae), for the territory of the EU. L. orbonalis is a tropical and sub-tropical species native to Asia and Australia with India considered its centre of origin. Following taxonomic revision, literature reporting L. orbonalis from sub-Saharan Africa should be regarded as referring to members of a complex of other species of Leucinodes native to Africa and not as referring to L. orbonalis. L. orbonalis is not present in the EU and is not a regulated EU pest. L. orbonalis is a major pest of Solanum melongena (eggplant) in Asia where larvae feed within leaves, stems, shoots and fruits. Larvae can also feed on a range of other plants, mostly within Solanaceae although L. orbonalis is generally not reported as a pest of crops other than S. melongena. However, in recent years L. orbonalis has emerged as a pest of Solanum tuberosum in south-west India. In tropical areas there can be 10 generations per year if conditions are suitable. L. orbonalis has been intercepted 350 times in the EU from a range of Asian countries on a range of produce, mostly larvae in fruits of S. melongena. Biotic factors (host availability) and abiotic factors (climate suitability) suggest that some small areas of the EU could be suitable for establishment. Adult L. orbonalis can fly and the species could spread within the EU. The introduction of L. orbonalis into the EU would have an economic impact, most likely on S. melongena production, the magnitude of which is uncertain. Measures are available to prevent the entry of L. orbonalis into the EU. L. orbonalis satisfies the criteria that are within the remit of EFSA to assess for this species to be regarded as a potential Union quarantine pest.

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Genome mining and functional analysis of cytochrome P450 genes involved in insecticide resistance in Leucinodes orbonalis (Lepidoptera: Crambidae)

Cited by 13 publications

References 56 publications

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

20E biosynthesis gene CYP306A1 confers resistance to imidacloprid in the nymph stage of Bemisia tabaci by detoxification metabolism

Genome Mining and Expression Analysis of Carboxylesterase and Glutathione S-Transferase Genes Involved in Insecticide Resistance in Eggplant Shoot and Fruit Borer, Leucinodes orbonalis (Lepidoptera: Crambidae)

Pest categorisation of Leucinodes orbonalis

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