Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-26T07:26:49.514Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic analysis and screening of detoxification-related genes in an amitraz-resistant strain of Panonychus citri

Published online by Cambridge University Press:  18 May 2020

Shi-Jiang Yu Open the ORCID record for Shi-Jiang Yu [Opens in a new window] ,
Lin Cong ,
Hao-Qiang Liu  and
Chun Ran Open the ORCID record for Chun Ran [Opens in a new window]
Shi-Jiang Yu
Affiliation:
Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, National Engineering Research Center for Citrus, Chongqing400712, China
Lin Cong
Affiliation:
Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, National Engineering Research Center for Citrus, Chongqing400712, China
Hao-Qiang Liu
Affiliation:
Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, National Engineering Research Center for Citrus, Chongqing400712, China
Chun Ran*
Affiliation:
Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, National Engineering Research Center for Citrus, Chongqing400712, China
*
Author for correspondence: Chun Ran, Email: ranchun@cric.cn
Get access Rights & Permissions [Opens in a new window]

Abstract

Panonychus citri (McGregor) is the most common pest in citrus-producing regions. Special low-toxicity acaricides, such as spirocyclic tetronic acids and mite growth inhibitors, have been used for a long time in China. However, pesticide resistance in mites is a growing problem due to the lack of new acaricide development. Wide-spectrum insecticides, such as amitraz have gained acceptance among fruit growers. An amitraz-resistant strain of P. citri was obtained by indoor screening to examine field resistance monitoring of mites to acaricides and to explore the resistant mechanism of mites against amitraz. The amitraz-resistant strain of P. citri had an LC50 value of 2361.45 mg l−1. The resistance ratio was 81.35 times higher in the resistant strain of P. citri compared with the sensitive strain. Crossing experiments between the sensitive and resistant strains of P. citri were conducted, resulting in a D value of 0.11 for F1 SS♀×RS♂ and 0.06 for F1 RS♀×SS♂. Reciprocal cross experiments showed that the dose–mortality curves for the F1 generations coincided, indicating that the resistance trait was not affected by cytoplasmic inheritance. The dose–expected response relationship was evaluated in the backcross generation and a significant difference was observed compared with the actual value. The above results indicate that the inheritance of resistance trait was incompletely dominant, governed by polygenes on the chromosome. Synergism studies demonstrated that cytochrome P450s and esterase may play important roles in the detoxification of amitraz. Based on differential gene analysis, 23 metabolism-related genes of P. citri were identified, consistent with the results of synergism studies. Real-time PCR verification implied that P450s, ABC transporters, and acetylcholinesterase might influence the detoxification of amitraz by P. citri. These results provide the genetic and molecular foundation for the management of pest mite resistance.

Keywords

Amitrazdetoxificationgenetic analysisPanonychus citriresistance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 6 , December 2020 , pp. 743 - 755
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Baron, S, Barrero, RA, Black, M, Bellgard, MI, van Dalen, E and Maritz-Olivier, C (2018) Differentially expressed genes in response to amitraz treatment suggests a proposed model of resistance to amitraz in R. decoloratus Ticks. International Journal for Parasitology: Drugs and Drug Resistance 8, 361–371.Google ScholarPubMed
Broehan, G, Kroeger, T, Lorenzen, M and Merzendorfer, H (2013) Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 14, 6.CrossRefGoogle ScholarPubMed
Buss, DS and Callaghan, A (2008) Interaction of pesticides with p-glycoprotein and other ABC proteins: a survey of the possible importance to insecticide, herbicide and fungicide resistance. Pesticide Biochemistry and Physiology 90, 141–153.CrossRefGoogle Scholar
Busvine, JR (1980) Revised method for spider mites and their eggs (e.g., Tetranychus App. and Panonychus ulmi Koch). FAO method No. 10a. In: recommended methods for measurement of pest resistance to pesticides. FAO Plant Production and Protection 21, 49–53.Google Scholar
Corley, SW, Jonsson, NN, Piper, EK, Cutullé, C, Stear, MJ and Seddon, JM (2013) Mutation in the RmßAOR gene is associated with amitraz resistance in the cattle tick Rhipicephalus microplus. Proceedings of the National Academy of Sciences of the USA 110, 16772–16777.CrossRefGoogle ScholarPubMed
David, FN and Lehmann, EL (1961) Testing statistical hypotheses. The Mathematical Gazette. Available at https://doi.org/10.2307/3614657.CrossRefGoogle Scholar
Demaeght, P, Dermauw, W, Tsakireli, D, Khajehali, J, Nauen, R, Tirry, L, Vontas, J, Lümmen, P and Van Leeuwen, T (2013) Molecular analysis of resistance to acaricidal spirocyclic tetronic acids in Tetranychus urticae: CYP392E10 metabolizes spirodiclofen, but not its corresponding enol. Insect Biochemistry and Molecular Biology 43, 544–554.CrossRefGoogle Scholar
Demaeght, P, Osborne, EJ, Odman-Naresh, J, Grbić, M, Nauen, R, Merzendorfer, H, Clark, RM and Van Leeuwen, T (2014) High resolution genetic mapping uncovers chitin synthase-1 as the target-site of the structurally diverse mite growth inhibitors clofentezine, hexythiazox and etoxazole in Tetranychus urticae. Insect Biochemistry and Molecular Biology 51, 52–61.CrossRefGoogle ScholarPubMed
Dermauw, W, Osborne, EJ, Clark, RM, Grbić, M, Tirry, L and Van Leeuwen, T (2013) A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genomics 14, 317.CrossRefGoogle ScholarPubMed
Heckel, DG (2012) Learning the ABCs of Bt: ABC transporters and insect resistance to Bacillus thuringiensis provide clues to a crucial step in toxin mode of action. Pesticide Biochemistry and Physiology 104, 103–110.CrossRefGoogle Scholar
Hu, J, Wang, C, Wang, J, You, Y and Chen, F (2010) Monitoring of resistance to spirodiclofen and five other acaricides in Panonychus citri collected from Chinese citrus orchards. Pest Management Science 66, 1025–1030.CrossRefGoogle ScholarPubMed
Huang, QT, Ma, HH, Deng, XL, Zhu, H, Liu, J, Zhou, Y and Zhou, XM (2018) Pharmacological characterization of a β-adrenergic-like octopamine receptor in Plutella xylostella. Archives of Insect Biochemistry and Physiology 98, e21466.CrossRefGoogle ScholarPubMed
Jagadeesan, R, Fotheringham, A, Ebert, PR and Schlipalius, DI (2013) Rapid genome wide mapping of phosphine resistance loci by a simple regional averaging analysis in the red flour beetle, Tribolium castaneum. BMC Genomics 14, 650.CrossRefGoogle ScholarPubMed
Jonsson, NN, Klafke, G, Corley, SW, Tidwell, J, Berry, CM and Caline, HKT (2018) Molecular biology of amitraz resistance in cattle ticks of the genus Rhipicephalus. Frontiers in Bioscience – Landmark 23, 796–810.CrossRefGoogle ScholarPubMed
Kita, T, Hayashi, T, Ohtani, T, Takao, H, Takasu, H, Liu, G, Ohta, H, Ozoe, F and Ozoe, Y (2017) Amitraz and its metabolite differentially activate α- and β-adrenergic-like octopamine receptors. Pest Management Science 73, 984–990.CrossRefGoogle ScholarPubMed
Koh-Tan, HHC, Strachan, E, Cooper, K, Bell-Sakyi, L and Jonsson, NN (2016) Identification of a novel β-adrenergic octopamine receptor-like gene (βAOR-like) and increased ATP-binding cassette B10 (ABCB10) expression in a Rhipicephalus microplus cell line derived from acaricide-resistant ticks. Parasites and Vectors 9, 425.CrossRefGoogle Scholar
Leng, N, Dawson, JA, Thomson, JA, Ruotti, V, Rissman, AI, Smits, BMG, Haag, JD, Gould, MN, Stewart, RM and Kendziorski, C (2013) EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics (Oxford, England) 29, 2073.CrossRefGoogle ScholarPubMed
Mangia, C, Vismarra, A, Genchi, M, Epis, S, Bandi, C, Grandi, G, Bell-Sakyi, L, Otranto, D, Passeri, B and Kramer, L (2018) Exposure to amitraz, fipronil and permethrin affects cell viability and ABC transporter gene expression in an Ixodes ricinus cell line. Parasites and Vectors 11, 437.CrossRefGoogle Scholar
Niu, JZ, Dou, W, Ding, TB, Yang, LH, Shen, GM and Wang, JJ (2012) Evaluation of suitable reference genes for quantitative RT-PCR during development and abiotic stress in Panonychus citri (McGregor) (Acari: Tetranychidae). Molecular Biology Reports 39, 5841–5849.CrossRefGoogle Scholar
Ouyang, Y, Montez, GH, Liu, L and Grafton-Cardwell, EE (2012) Spirodiclofen and spirotetramat bioassays for monitoring resistance in citrus red mite, Panonychus citri (Acari: Tetranychidae). Pest Management Science 68, 781–787.CrossRefGoogle Scholar
Park, Y, González-Martínez, RM, Navarro-Cerrillo, G, Chakroun, M, Kim, Y, Ziarsolo, P, Blanca, J, Cañizares, J, Ferré, J and Herrero, S (2014) ABCC transporters mediate insect resistance to multiple Bt toxins revealed by bulk segregant analysis. BMC Biology 12, 46.CrossRefGoogle ScholarPubMed
Pfaffl, MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.CrossRefGoogle ScholarPubMed
Preisler, HK, Hoy, MA and Robertson, JL (1990) Statistical analysis of modes of inheritance for pesticide resistance. Journal of Economic Entomology 83, 1649–1655.CrossRefGoogle Scholar
Ran, C, Chen, Y and Wang, JJ (2009) Susceptibility and carboxylesterase activity of five field populations of Panonychus citri (McGregor) (Acari: Tetranychidae) to four acaricides. International Journal of Acarology 35, 115–121.CrossRefGoogle Scholar
Snoeck, S, Greenhalgh, R, Tirry, L, Clark, RM, Van Leeuwen, T and Dermauw, W (2017) The effect of insecticide synergist treatment on genome-wide gene expression in a polyphagous pest. Scientific Reports 7, 13440.CrossRefGoogle Scholar
Snoeck, S, Kurlovs, AH, Bajda, S, Feyereisen, R, Greenhalgh, R, Villacis-Perez, E, Kosterlitz, O, Dermauw, W, Clark, RM and Van Leeuwen, T (2019) High-resolution QTL mapping in Tetranychus urticae reveals acaricide-specific responses and common target-site resistance after selection by different METI-I acaricides. Insect Biochemistry and Molecular Biology 110, 19–33.CrossRefGoogle ScholarPubMed
Stone, BF (1968) A formula for determining degree of dominance in cases of monofactorial inheritance of resistance to chemicals. Bulletin of the World Health Organization 38, 325.Google Scholar
Trapnell, C, Williams, BA, Pertea, G, Mortazavi, A, Kwan, G, Van Baren, MJ, Salzberg, SL, Wold, BJ and Pachter, L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology 28, 511–U174.CrossRefGoogle ScholarPubMed
Van Leeuwen, T and Dermauw, W (2016) The molecular evolution of xenobiotic metabolism and resistance in chelicerate mites. Insect Biochemistry and Molecular Biology 61, 475.Google ScholarPubMed
Van Leeuwen, T, Stillatus, V and Tirry, L (2004) Genetic analysis and cross-resistance spectrum of a laboratory-selected chlorfenapyr resistant strain of two-spotted spider mite (Acari: Tetranychidae). Experimental and Applied Acarology 32, 249–261.CrossRefGoogle Scholar
Van Leeuwen, T, Vontas, J, Tsagkarakou, A, Dermauw, W and Tirry, L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochemistry and Molecular Biology 40, 563–572.CrossRefGoogle ScholarPubMed
Van Leeuwen, T, Van Nieuwenhuyse, P, Vanholme, B, Dermauw, W, Nauen, R and Tirry, L (2011) Parallel evolution of cytochrome b mediated bifenazate resistance in the citrus red mite Panonychus citri. Insect Molecular Biology 20, 135–140.CrossRefGoogle ScholarPubMed
Van Leeuwen, T, Demaeght, P, Osborne, EJ, Dermauw, W, Gohlke, S, Nauen, R, Grbić, M, Tirry, L, Merzendorfer, H and Clark, RM (2012) Population bulk segregant mapping uncovers resistance mutations and the mode of action of a chitin synthesis inhibitor in arthropods. Proceedings of the National Academy of Sciences of the USA 109, 4407–4412.CrossRefGoogle ScholarPubMed
Van Leeuwen, T, Tirry, L, Yamamoto, A, Nauen, R and Dermauw, W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pesticide Biochemistry and Physiology 121, 12–21.CrossRefGoogle Scholar
Van Pottelberge, S, Van Leeuwen, T, Khajehali, J and Tirry, L (2009a) Genetic and biochemical analysis of a laboratory-selected spirodiclofen-resistant strain of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Management Science 65, 358–366.CrossRefGoogle Scholar
Van Pottelberge, S, Van Leeuwen, T, Nauen, R and Tirry, L (2009b) Resistance mechanisms to mitochondrial electron transport inhibitors in a field-collected strain of Tetranychus urticae Koch (Acari: Tetranychidae). Bulletin of Entomological Research 99, 23–31.CrossRefGoogle Scholar
Yamamoto, A, Yoneda, H, Hatano, R and Asada, M (1996) Stability of hexythiazox resistance in the citrus red mite, Panonychus citri (McGregor) under laboratory and field conditions. Journal of Pesticide Science 21, 37–42.CrossRefGoogle Scholar
Yu, S, Ding, L, Luo, R, Li, X, Yang, J, Liu, H, Cong, L and Ran, C (2016) Identification of immunity-related genes in Dialeurodes citri against entomopathogenic fungus Lecanicillium attenuatum by rnaseq analysis. PLoS ONE 11, e0162659.CrossRefGoogle Scholar
Supplementary material: File

Yu et al. supplementary material

Tables S1-S2 and Figure S1

Download Yu et al. supplementary material(File)
File 196 KB