Global transcriptome profiling and functional analysis reveal that tissue-specific constitutive overexpression of cytochrome P450s confers tolerance to imidacloprid in palm weevils in date palm fields.
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Type
ArticleKAUST Department
Bioscience ProgramBiological and Environmental Sciences and Engineering (BESE) Division
KAUST Grant Number
BAS/1/1020-01-01Date
2019-05-31Online Publication Date
2019-05-31Print Publication Date
2019-12Permanent link to this record
http://hdl.handle.net/10754/656354
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BACKGROUND:Cytochrome P450-dependent monooxygenases (P450s), constituting one of the largest and oldest gene superfamilies found in many organisms from bacteria to humans, play a vital role in the detoxification and inactivation of endogenous toxic compounds. The use of various insecticides has increased over the last two decades, and insects have developed resistance to most of these compounds through the detoxifying function of P450s. In this study, we focused on the red palm weevil (RPW), Rhynchophorus ferrugineus, the most devastating pest of palm trees worldwide, and demonstrated through functional analysis that upregulation of P450 gene expression has evolved as an adaptation to insecticide stress arising from exposure to the neonicotinoid-class systematic insecticide imidacloprid. RESULTS:Based on the RPW global transcriptome analysis, we identified 101 putative P450 genes, including 77 likely encoding protein coding genes with ubiquitous expression. A phylogenetic analysis revealed extensive functional and species-specific diversification of RPW P450s, indicating that multiple CYPs actively participated in the detoxification process. We identified highly conserved paralogs of insect P450s that likely play a role in the development of resistance to imidacloprid: Drosophila Cyp6g1 (CYP6345J1) and Bemisia tabaci CYP4C64 (CYP4LE1). We performed a toxicity bioassay and evaluated the induction of P450s, followed by the identification of overexpressed P450s, including CYP9Z82, CYP6fra5, CYP6NR1, CYP6345J1 and CYP4BD4, which confer cross-resistance to imidacloprid. In addition, under imidacloprid insecticide stress in a date palm field, we observed increased expression of various P450 genes, with CYP9Z82, CYP4BD4, CYP6NR1 and CYP6345J1 being the most upregulated detoxification genes in RPWs. Expression profiling and cluster analysis revealed P450 genes with multiple patterns of induction and differential expression. Furthermore, we used RNA interference to knock down the overexpressed P450s, after which a toxicity bioassay and quantitative expression analysis revealed likely candidates involved in metabolic resistance against imidacloprid in RPW. Ingestion of double-stranded RNA (dsRNA) successfully knocked down the expression of CYP9Z82, CYP6NR1 and CYP345J1 and demonstrated that silencing of CYP345J1 and CYP6NR1 significantly decreased the survival rate of adult RPWs treated with imidacloprid, indicating that overexpression of these two P450s may play an important role in developing tolerance to imidacloprid in a date palm field. CONCLUSION:Our study provides useful background information on imidacloprid-specific induction and overexpression of P450s, which may enable the development of diagnostic tools/markers for monitoring the spread of insecticide resistant RPWs. The observed trend of increasing tolerance to imidacloprid in the date palm field therefore indicated that strategies for resistance management are urgently needed.Citation
Antony, B., Johny, J., Abdelazim, M. M., Jakše, J., Al-Saleh, M. A., & Pain, A. (2019). Global transcriptome profiling and functional analysis reveal that tissue-specific constitutive overexpression of cytochrome P450s confers tolerance to imidacloprid in palm weevils in date palm fields. BMC Genomics, 20(1). doi:10.1186/s12864-019-5837-4Sponsors
We thank the date palm farmers in the Al Qassim area for support in obtaining red palm weevils and advice in adult weevil collection. We thank the KSU - Deanship of Scientific Research, Research Chair Program, Saudi Arabia. The authors are grateful to Dr. David. R. Nelson (University of Tennessee) for the P450 nomenclature. JJ is thankful for a researcher stipend obtained from the 12-AGR2554-02 project. We also thank Samy M. Mustafa of CDPR, Dr. Asma A. Al-Nujiban of Qassim University, Dr. Saleh. A. Aldosari and Mr. Waheed M. Alraha of CDPR for providing technical support and conducting RPW field collection. We are grateful to the editor and reviewers for their numerous perceptive and constructive comments, which helped us to improve our manuscript.Funding: Funding for this research (awarded to BA) (Grant no. KACST-NSTIP 12-AGR2554–02) was provided by the National Plan for Science, Technology and Innovation (MAARIFAH) of King Abdul Aziz City for Science and Technology (KACST), Kingdom of Saudi Arabia. The authors are grateful to the Deanship of Scientific Research, King Saud University for funding through the Vice Deanship of Scientific Research Chairs. The transcriptome data were generated using faculty baseline funding from the King Abdullah University of Science and Technology (KAUST) to AP (BAS/1/1020-01-01). The funders had no role in study design, data collection and analysis, and interpretation of data and preparation of the manuscript.
Publisher
Springer Science and Business Media LLCJournal
BMC genomicsRelations
Is Supplemented By:- [Dataset]
Binu Antony, Jibin Johny, Abdelazim, M., JakĹĄe, J., Al-Saleh, M., & Arnab Pain. (2019). Global transcriptome profiling and functional analysis reveal that tissue-specific constitutive overexpression of cytochrome P450s confers tolerance to imidacloprid in palm weevils in date palm fields. Figshare. https://doi.org/10.6084/M9.FIGSHARE.C.4526078.V1. DOI: 10.6084/m9.figshare.c.4526078.v1 Handle: 10754/664754
ae974a485f413a2113503eed53cd6c53
10.1186/s12864-019-5837-4
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