Abstract
The citrus red mite, Panonychus citri, is one of the most economically and globally destructive mite pests of citrus. Acaricide resistance has been a growing problem in controlling this pest. As the main inhibitory neurotransmitter in organisms, γ-aminobutyric acid (GABA) is synthesized from the amino acid glutamate by the action of glutamate decarboxylases (GADs). In the present study, one novel GAD gene, PcGAD, was identified and characterized from P. citri. The opening reading frame of PcGAD contained 1548 nucleotides that encode 515 amino acids. The subsequent spatiotemporal expression pattern by RT-qPCR revealed that the expression levels of PcGAD were significantly higher in larvae than in adults. Challenging with various concentrations of abamectin resulted in the upregulation of PcGAD transcript levels. Furthermore, biochemical characterization indicated that changes in GAD activity coincided with its mRNA levels. High-performance liquid chromatography confirmed that the GABA contents of P. citri increased upon abamectin treatment. The application of abamectin induces PcGAD expression and activates GAD activity, thereby resulting in an increase in GABA content in P. citri, which contributes to the adaptability of the mite to abamectin challenge.
Access this article
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
Similar content being viewed by others
References
Bairoch A (1993) The PROSITE dictionary of sites and patterns in proteins, its current status. Nucleic Acids Res 21:3097
Bansal R, Hulbert S, Schemerhorn B, Reese JC, Whitworth RJ, Stuart JJ, Chen MS (2011) Hessian fly-associated bacteria: transmission, essentiality, and composition. PLoS ONE 6:e23170
Bormann J (2000) The ‘ABC’ of GABA receptors. Trends Pharmacol Sci 21:16–19
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Buckingham SD, Biggin PC, Sattelle BM, Brown LA, Sattelle DB (2005) Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol Pharmacol 68:942–951
Casida JE, Durkin KA (2015) Novel GABA receptor pesticide targets. Pestic Biochem Physiol 121:22–30
Dermauw W, Ilias A, Riga M, Tsagkarakou A, Grbic M, Tirry L, Van Leeuwen T, Vontas J (2012) The cys-loop ligand-gated ion channel gene family of Tetranychus urticae: implications for acaricide toxicology and a novel mutation associated with abamectin resistance. Insect Biochem Mol Biol 42:455–465
Dermauw W, Osborne EJ, Clark RM, Grbić M, Tirry L, Van Leeuwen T (2013) A burst of ABC genes in the genome of the polyphagous spider mite Tetranychus urticae. BMC Genom 14:317
Ding TB, Niu JZ, Yang LH, Zhang K, Dou W, Wang JJ (2013) Transcription profiling of two cytochrome P450 genes potentially involved in acaricide metabolism in citrus red mite Panonychus citri. Pestic Biochem Physiol 106:28–37
Dyrløv Bendtsen J, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795
Fenalti G, Law RHP, Buckle AM, Langendorf C, Tuck K, Rosado CJ, Faux NG, Mahmood K, Hampe CS, Banga JP, Wilce M, Schmidberger J, Rossjohn J, El-Kabbani O, Pike RN, Smith AI, Mackay IR, Rowley MJ, Whisstock JC (2007) GABA production by glutamic acid decarboxylase is regulated by a dynamic catalytic loop. Nat Struct Mol Biol 14:280–286
Geary T (2005) Ivermectin 20 years on: maturation of a wonder drug. Trends Parasitol 21:530–532
Grone BP, Maruska KP (2016) Three distinct glutamate decarboxylase genes in vertebrates. Sci Rep 6:30507
He L, Xue CH, Wang JJ, Li M, Lu WC, Zhao ZM (2009) Resistance selection and biochemical mechanism of resistance to two acaricides in Tetranychus cinnabarinus (Boisduval). Pestic Biochem Physiol 93:47–52
Hu J, Wang C, Wang J, You Y, Chen F (2010) Monitoring of resistance to spirodiclofen and five other acaricides in Panonychus citri collected from Chinese citrus orchards. Pest Manag Sci 66:1025–1030
Huang J, Casida JE (1997) Avermectin B1a binds to high- and low-affinity sites with dual effects on the γ-aminobutyric acid-gated chloride channel of cultured cerebellar granule neurons. J Pharmacol Exp Ther 281:261–266
Ilg T, Berger M, Noack S, Rohwer A, Gaßel M (2013) Glutamate decarboxylase of the parasitic arthropods Ctenocephalides felis and Rhipicephalus microplus: gene identification, cloning, expression, assay development, identification of inhibitors by high throughput screening and comparison with the orthologs from Drosophila melanogaster and mouse. Insect Biochem Mol Biol 43:162–177
Kane NS, Hirschberg B, Qian S, Hunt D, Thomas B, Brochu R, Ludmerer SW, Zheng Y, Smith M, Arena JP, Cohen CJ, Schmatz D, Warmke J, Cully DF (2000) Drug-resistant Drosophila indicate glutamate-gated chloride channels are targets for the antiparasitics nodulosporic acid and ivermectin. Proc Natl Acad Sci USA 97:13949–13954
Kehoe J, Buldakova S, Acher F, Dent J, Bregestovski P, Bradley J (2009) Aplysia cys-loop glutamate-gated chloride channels reveal convergent evolution of ligand specificity. J Mol Evol 69:125–141
Kim JI, Ganesan S, Luo SX, Wu YW, Park E, Huang EJ, Chen L, Ding JB (2015) Aldehyde dehydrogenase 1a1 mediates a GABA synthesis pathway in midbrain dopaminergic neurons. Science 350:102–106
Kwon DH, Im JS, Ahn JJ, Lee JH, Clark JM, Lee SH (2010) Acetylcholinesterase point mutations putatively associated with monocrotophos resistance in the two-spotted spider mite. Pestic Biochem Physiol 96:36–42
Liao CYWK, Xia YC, Feng G, Li H, Liu W, Dou JJ Wang (2016) Characterization and functional analysis of a novel glutathione S-transferase gene potentially associated with the abamectin resistance in Panonychus citri (McGregor). Pestic Biochem Physiol 132:72–80
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using Real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408
Luo L, Sun YJ, Wu YJ (2013) Abamectin resistance in Drosophila is related to increased expression of P-glycoprotein via the dEGFR and dAkt pathways. Insect Biochem Mol Biol 43:627–634
Niu JZ, Dou W, Ding TB, Shen GM, Zhang K, Smagghe G, Wang JJ (2012a) Transcriptome analysis of the citrus red mite, Panonychus citri, and its gene expression by exposure to insecticide/acaricide. Insect Mol Biol 21:422–436
Niu JZ, Dou W, Ding TB, Yang LH, Shen GM, Wang JJ (2012b) Evaluation of suitable reference genes for quantitative RT-PCR during development and abiotic stress in Panonychus citri (McGregor) (Acari: Tetranychidae). Mol Biol Rep 39:5841–5849
Park KB, Oh SH (2007) Cloning, sequencing and expression of a novel glutamate decarboxylase gene from a newly isolated lactic acid bacterium, Lactobacillus brevis OPK-3. Bioresour Technol 98:312–319
Pavlidi N, Tseliou V, Riga M, Nauen R, Van Leeuwen T, Labrou NE, Vontas J (2015) Functional characterization of glutathione S-transferases associated with insecticide resistance in Tetranychus urticae. Pestic Biochem Physiol 121:53–60
Pu X, Yang YH, Wu SW, Wu YD (2010) Characterisation of abamectin resistance in a field-evolved multiresistant population of Plutella xylostella. Pest Manag Sci 66:371–378
Putter I, Macconnell JG, Preiser FA, Haidri AA, Ristich SS, Dybas RA (1981) Avermectins: novel insecticides, acaricides and nematicides from a soil microorganism. Experientia 37:963–964
Riga M, Tsakireli D, Ilias A, Morou E, Myridakis A, Stephanou E, Nauen R, Dermauw W, Van Leeuwen T, Paine M, Vontas J (2014) Abamectin is metabolized by CYP392A16, a cytochrome P450 associated with high levels of acaricide resistance in Tetranychus urticae. Insect Biochem Mol Biol 46:43–53
Rubio LA (2003) Determination of diaminopimelic acid in rat feces by high-performance liquid chromatography using the Pico Tag method. J Chromatogr B 784:125–129
Salat K, Kulig K (2011) GABA transporters as targets for new drugs. Future Med Chem 3:211–222
Sanyanarayan V, Nair PM (1985) Purification and characterization of glutamate decarboxylase from Solanum tuberosum. Eur J Biochem 150:53–60
Scott JG, Roush RT, Liu N (1991) Selection of high-level abamectin resistance from field-collected house flies, Musca domestica. Cell Mol Life Sci 47:288–291
Stumpf N, Nauen R (2002) Biochemical markers linked to abamectin resistance in Tetranychus urticae (Acari: Tetranychidae). Pestic Biochem Physiol 72:111–121
Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572
Van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Physiol 121:12–21
Wang LH, Wu YD (2007) Cross-resistance and biochemical mechanisms of abamectin resistance in the B-type Bemisia tabaci. J Appl Entomol 131:98–103
Wei D, Wang T, Dou W, Wang JJ (2014) Biochemical and molecular characteristics of glutamic decarboxylase from Bactrocera dorsalis. Agric Sci China 47:3184–3194
Wolstenholme AJ, Rogers AT (2005) Glutamate-gated chloride channels and the mode of action of the avermectin/milbemycin anthelmintics. Parasitology 131:S85–S95
Xia WK, Ding TB, Niu JZ, Liao CY, Zhong R, Yang WJ, Liu B, Dou W, Wang JJ (2014) Exposure to diflubenzuron results in an up-regulation of a chitin synthase 1 gene in citrus red mite, Panonychus citri (Acari: Tetranychidae). Int J Mol Sci 15:3711–3728
Zhu XJ, Lu WC, Feng YN, He L (2010) High γ-aminobutyric acid content, a novel component associated with resistance to abamectin in Tetranychus cinnabarinus (Boisduval). J Insect Physiol 56:1895–1900
Acknowledgements
This research was supported in part by Special Funds for Agro-Scientific Research and Grain Scientific Research in the Public Interest (201203038, 201413007-2), the National Natural Science Foundation (31672049), Chongqing Research Program of Basic Research and Frontier Technology (CSTC, 2015jcyjBX0061), and the earmarked fund for the Modern Agro-industry (Citrus) Technology Research System of China (CARS-27).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dou, W., Xia, WK., Niu, JZ. et al. Abamectin treatment affects glutamate decarboxylase expression and induces higher GABA levels in the citrus red mite, Panonychus citri . Exp Appl Acarol 72, 229–244 (2017). https://doi.org/10.1007/s10493-017-0150-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-017-0150-x